Download Episodic autobiographical memories over the course of time

G Model
ARTICLE IN PRESS
NSY-3193; No. of Pages 16
Neuropsychologia xxx (2009) xxx–xxx
Contents lists available at ScienceDirect
Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia
Episodic autobiographical memories over the course of time:
Cognitive, neuropsychological and neuroimaging findings
Pascale Piolino a,b,c,∗ , Béatrice Desgranges c , Francis Eustache c
a
b
c
Université Paris Descartes, Institut de Psychologie, Paris, France
CNRS, UMR 8189, Laboratoire Psychologie et Neurosciences Cognitives, Paris, France
Inserm-EPHE-Université de Caen/Basse-Normandie, Unité U923, GIP Cyceron, CHU Côte de Nacre, Caen, France
a r t i c l e
i n f o
Article history:
Received 17 September 2008
Received in revised form 1 December 2008
Accepted 11 January 2009
Available online xxx
Keywords:
Consciousness
Consolidation
Retrieval
Remembering/knowing
Hippocampus
Prefrontal cortex
Temporal lobe
a b s t r a c t
The critical attributes of episodic memory are self, autonoetic consciousness and subjectively sensed time.
The aim of this paper is to present a theoretical overview of our already published researches into the
nature of episodic memory over the course of time. We have developed a new method of assessing autobiographical memory (TEMPau task), which is specially designed to measure these specific aspects, based
on the sense of re-experiencing events from across the entire lifespan. Based on our findings of cognitive,
neuropsychological and neuroimaging studies, new insights into episodic autobiographical memories are
presented, focusing on the effects of age of the subjects interacting with time interval in healthy subjects
and lesioned patients. The multifaceted and complex nature of episodic memory is emphasized and it
is suggested that mental time travel through subjective time, which allows individuals to re-experience
specific past events through a feeling of self-awareness, is the last feature of autobiographical memory
to become fully operational in development and the first feature to go in aging and most amnesias. Our
findings highlight the critical role of frontotemporal areas in constructive autobiographical memory processes, and especially hippocampus, in re-experiencing episodic details from the recent or more distant
past.
© 2009 Published by Elsevier Ltd.
“Yesterday evening, as I was taking a solitary walk . . .; I was
roused from my thoughts by the warbling of a thrush perched
on the uppermost branch of a birch. At that very instant, its
magic notes conjured up images of the family estate . . . suddenly transported back into the past, I gazed once more upon the
countryside where I had so often heard the thrush’s song. When
I listened to it then, I was as sad as I am now.” (Chateaubriand,
Mémoire d’outre tombe [Memoirs from beyond the tomb], 1848)
1. The concept of lifelong episodic autobiographical
memory
In previous centuries, philosophers and psychologists regarded
memory as a power of the mind responsible for our self-identity
(e.g. James, 1890; Locke, 1690). It was a unique property, as illustrated by Théodule Ribot (1881): “I have made the journey from
Paris to Brest a hundred times. All these images overlap to form
an unclear mass—a single, vague state, if the truth be told. Of all
these journeys, only those connected to some important event, be
∗ Corresponding author at: 71 avenue Edouard Vaillant, 92774 BoulogneBillancourt, France. Tel.: +33 1 55 20 59 22; fax: +33 1 55 20 58 53.
E-mail address: [email protected] (P. Piolino).
it happy or unfortunate, appear to me as memories: only those that
arouse secondary states of consciousness are situated in time.” In
the same vein, James (1890) emphasized that “memory requires
more than mere dating of a fact in the past. It must be dated
in my past. In other words, I must think that I directly experienced its occurrence. It must have that “warmth and intimacy”
. . . as characterizing all experiences “appropriated” by the thinker
as his own” (volume I, p. 650). This view closely parallels current
conceptions of episodic memory, placing an emphasis on the subjective recollective experience and on pastness. The ambition of
this paper is to present a theoretical overview into the multifaceted
and complex nature of episodic memory emphasizing its temporal
complexity, i.e. changes with the age of subjects, interacting with
the age of memories, based on our already published researches in
terms of cognitive, neuropsychological, and functional neuroimaging approaches.
According to its most recent definition, episodic memory refers
to personal events recollected in the context of a particular time
and place – the “what”, “where” and “when” – and with some reference to oneself as a participant in the episode (Tulving, 1985,
2001, 2002). With the development of the theory of episodic memory, the essence of this memory system has shifted away from
specificity and towards the phenomenal experience of remembering (Brewer, 1996; Baddeley, 2001; Gardiner, 2001; Tulving, 2001,
0028-3932/$ – see front matter © 2009 Published by Elsevier Ltd.
doi:10.1016/j.neuropsychologia.2009.01.020
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
2
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
2002; Wheeler, Stuss, & Tulving, 1997). As such, it encompasses perceptual, affective and spatiotemporal contextual details, and gives
the rememberer the feeling that a representation is the recollection of an event belonging to his or her personal past. Although
this memory system contrasts with semantic memory, its operations rely on, but go beyond, the semantic memory system. Episodic
and semantic memory systems are associated with two distinct
states of consciousness: autonoetic and noetic consciousness. Autonoetic consciousness, which is a sine qua non of episodic memory,
is defined by a sense of self in time and the mental reliving of subjective experiences arising from the encoding context. Hence, based
on a combination of self, autonoetic consciousness and subjectively
sensed time, episodic memory makes it possible to travel mentally
through subjective time, from present to past, and thus to recollect, one’s own previous experiences via autonoetic consciousness.
The central tenet of this theory therefore revolves around phenomenological re-experiencing and the sense of self in time. The
neural bases of episodic memory and autonoetic consciousness are
thought to be subserved primarily by the prefrontal cortex, but also
by the medial temporal lobe (Tulving & Markowitsch, 1998; VarghaKhadem et al., 1997). By contrast, semantic memory is associated
with noetic consciousness, which denotes the subject’s ability to
be aware of information about the world in the absence of any
remembering, and is subserved by a broad set of neocortical areas
(including frontal, temporal and occipital cortices).
As episodic memory refers to events recollected in the context
of a particular time and place, and with a degree of autobiographical reference, autobiographical memory (AM) has long been
regarded as being episodic in nature. Moreover, autobiographical memory gives researchers the opportunity to study episodic
memory using self-relevant material that is more closely related
to the current definition of episodic memory (Tulving, 2001, 2002)
than that used in most standard tests of episodic memory (Piolino,
2008). The latter rarely make a distinction between the different components (content and context) of episodic memory and
do not measure very lengthy retention intervals, autobiographical
references or rich phenomenological and idiosyncratic aspects of
memory. Interestingly, the assessment of autobiographical memory makes it possible to investigate not only the ability to recall
a specific and meaningful personal event, locating it in time and
space, but also the ability to travel back into the past and relive
specific details of that event which distinguish it from any similar ones. However, as has so often happened in the history of
memory conceptions (Baddeley, 2001; Scoville & Milner, 1957),
neuropsychological examinations of patients have proved to be
an additional source of evidence. Drawing on their pioneering
study of the amnesic patient KC, Tulving, Schacter, McLachlan and
Moscovitch (Tulving, Schacter, McLachlan, & Moscovitch, 1988; see
Rosenbaum et al., 2005, for a review) were among the first to propose a clear distinction between the episodic component of AM
(disturbed in KC), containing personal specific events situated in
time and space, and a semantic component (preserved in KC), storing general knowledge about one’s past, such as the names of
acquaintances, personal addresses, generic events and self-concept
(Tulving, 1993). This study provided evidence that people can gain
mental access to their personal past not only through autonoetic
remembering but also through just knowing. Accordingly, semantic memory includes not only general information about the world,
but also knowledge about previous personal events and experiences
that one can no longer remember. More recently, Conway, Singer,
and Tagini (2004) claimed that the retrieval of autobiographical
memories depends on a complex, self-driven set of control processes and involves the episodic memory system, which contains
event-specific sensory–perceptual–cognitive–affective details, and
the long-term semantic self, which contains more abstract
autobiographical knowledge (i.e. generic events and conceptual
knowledge). Therefore, autobiographical memory is now recognized as being multifaceted, containing a body of general
knowledge, as well as unique experiences specific to an individual,
which have been accumulated since childhood, and which allow
him/her to construct a feeling of identity and continuity (Conway
& Pleydell-Pearce, 2000; Piolino, Desgranges, & Eustache, 2000;
Wilson & Ross, 2003). When it comes to the relationship between
self and memory, Tulving’s conception emphasizes the episodic
aspects of the self, defending the role of a phenomenological self in
the construction and maintenance of subjective continuity in time
and personal identity.
The episodic component of AM contains specific personal
events, with phenomenological details situated in time and space
pertaining to one’s self, and presupposes very lengthy retention
intervals. Its essence lies in the autonoetic state of consciousness,
which enables a personal event to be consciously recollected in its
original encoding context and implies mental time travel. Episodic
AMs have several core characteristics: they not only concern
unique, personal events situated in time and space, but also presuppose phenomenological details (i.e. perceptual, cognitive, affective
internal contextual details), self-relevance, the conscious recollection of these events and the rememberer’s personal perspective
(Brewer, 1996). Visual mental imagery and emotional experience are critical phenomenological characteristics of episodic AM
retrieval. Hence, the subjective sense of remembering almost
invariably involves some sort of visual (Greenberg & Rubin, 2003)
and emotional (Rubin & Berntsen, 2003) re-experiencing of an
event. Unlike episodic AM, the semantic component of AM is characterized by a noetic state of consciousness, in which one is capable
of retrieving general facts about personal events, but not of reexperiencing specific contexts. Therefore, not all memories that are
autobiographical have an autonoetic character mediated by the
episodic memory system.
One of the most interesting current debates about episodic
memory revolves around whether and how memories change over
time. One of the merits of AM studies is that they have painted
a much more dynamic picture of memory consolidation, storage
and retrieval than strictly “experimental” studies, i.e. those in the
Ebbinghaus tradition. There is a strong body of evidence that,
rather than being only determined by the length of the retention
interval, the distribution of episodic AMs across a long lifespan
reflects the survival of vivid memories from late adolescence and
early adulthood compared with other remote periods – the socalled reminiscence bump (Rubin, Wetzler, & Nebes, 1986; Rubin &
Schulkind, 1997; Rubin, Rahhal, & Poon, 1998) – which represents
a potent landmark for the current self (Conway & Pleydell-Pearce,
2000), serving to maintain a sense of identity and continuity in the
present. Furthermore, with the passage of time and the repetition of
similar events in the phenomenal experience of remembering realworld events, there is a shift away from autonoetic consciousness
and towards noetic consciousness, i.e. from episodic to semantic memory (Conway, Gardiner, Perfect, Anderson, & Cohen, 1997;
Robinson & Swanson, 1993). This shift is in line with the idea
that most features of very long-term memories become semanticized over time (Cermak, 1984), becoming a mixture of semantic
knowledge and specific experiences (see also Piolino, Lamidey,
Desgranges, & Eustache, 2007; Westmacott & Moscovitch, 2003 for
an illustration of this concept in the recollection of names of contemporary celebrities). The nature of AM retrieval and conscious
experience depends on the ratio of episodic to semantic elements
(see Cabeza & St Jacques, 2007, for a similar view). It has been postulated that the loss of episodic details and the emergence of a
conceptual organization cause a “Remember-to-Know” shift over
time, as a result of repeated encounters with similar events. It is
worth noting that repetition has been shown to influence autobiographical recollection, whether it be “internal” repetition (thinking
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
or talking about the same event) or “external” repetition (living
through similar events). While external repetition can lead to the
decontextualisation or semantization of events, internal repetition
can reinforce the persistence of phenomenological details over time
(Nadel, Campbell, & Ryan, 2007; Rubin & Kozin, 1984).
The nature of AM across lifetime periods is a critical aspect
of the lively argument about the neural substrates of long-term
memory consolidation. Despite numerous neuropsychological and
functional neuroimaging studies, the neurobiological bases of longterm episodic memory consolidation are still subject to debate
(Bright et al., 2006; Mc Gaugh, 2000; Meeter & Murre, 2004). There
are two main opposing theories regarding the involvement of the
medial temporal lobe (MTL) in long-term memory consolidation.
According to the Standard Theory (Bayley, Gold, Hopkins, & Squire,
2005; Squire & Alvarez, 1995), the MTL is involved in the storage
and retrieval of declarative memory (either semantic or episodic)
for a limited period of a few years. Direct connections have been
established between this model and the theory of episodic memory semanticization (see above, e.g. Eustache et al., 2004). The
main arguments of the Standard Theory are based on evidence
from neuropsychological studies showing diverse profiles of retrograde amnesia depending on the locus of the lesion. In amnesic
syndromes where the lesions are concentrated in the MTL or connected regions, the pattern of retrograde amnesia is consistent with
the Standard Theory and obeys Ribot’s Law (Ribot, 1881), with old
memories being better preserved than recent ones. The alternative Multiple Trace Theory considers that while the standard view
is valid for semantic information and semanticized memories over
time, it is not for lifelong episodic memories (Moscovitch et al.,
2005; Nadel & Moscovitch, 1997; Nadel, Campbell, et al., 2007).
Rather, the MTL continues to perform its task of recollecting the
myriad attributes (time, place, emotional content and perceptual
features) of episodic memories no matter how old they are.
Thus, given the multifaceted nature of AM, it is vital to have
stringent methods of investigation, especially in order to assess the
existence of episodic AM across different time periods, checking not
only the ability to represent a specific event and locate it in time and
space, but also the ability to recollect specific features of that event
via autonoetic consciousness (Moscovitch et al., 2005). In order to
investigate the complexity of episodic AM over the course of time
and to test the two conflicting models of long-term memory consolidation with respect to the MTL’s role in episodic memory retrieval,
we carried out a series of cognitive, neuropsychological and neuroimaging studies, using a new tool that has been specially designed
to measure the multifaceted episodic features of autobiographical
memories and the sense of recollection.
2. A new episodic autobiographical memory assessment
based on a subjective sense of recollection: the TEMPau task
Since Crovitz and Schiffmann’s ground-breaking study (1974),
the introduction of more fine-grained conceptions of AM has considerably improved the way we measure the various contents
of AM. However, far too few of the AM assessment tasks currently used in neuropsychology apply a definition of episodic AM
based on recollective experience, in accordance with Tulving’s current theories. Aside from techniques based on the Galton–Crovitz
cue-word paradigm, standardised semi-structured interviews have
been developed to examine AMs from different lifetime periods (e.g.
Borrini, Dall’Ora, Della Sala, Marinelli, & Spinnler, 1989; Ivaniou,
Cooper, Shanks, & Venneri, 2006; Kopelman, Wilson, & Baddeley,
1989). The scoring for autobiographical incidents revolves around
the specificity of the event recalled in time and place, and the richness of the description. This kind of scoring adheres to the definition
of episodic memory based on its “what,” “where” and “when” contents, but ignores the notion of mentally travelling back in time to
3
relive elements of the original experience. Thus, other decisive factors are generally needed to capture the “true” episodic attributes
of AM. Some researchers have attempted to unravel the subcomponents of AM, as defined by Tulving, according to the number of
contextual details. They claim that in addition to the specificity of
the recollection, it is the number of contextual details that makes
AM “truly episodic in the sense that one can literally re-experience
it” (Moscovitch, Yaschyshyn, Ziegler, & Nadel, 1999; p. 338). In
the same vein, Levine, Svoboda, Hay, Winocur, and Moscovitch
(2002) proposed investigating recollections from five different lifetime periods, separating the episodic from the non-episodic details
(repeated or factual details, metacognitive statements, etc.) by
means of a scoring procedure adapted from the Memory Characteristics Questionnaire created by Johnson, Foley, Suengas, & Raye
(1988), which lists the qualitative characteristics (e.g. perceptual,
spatiotemporal, and emotional) of details about personal events.
Particular attention is given to internal episodic details that are
regarded as reflecting autonoetic experience of the original event.
Interestingly, this procedure allows the fine-grained consideration
of both episodic and semantic features, even when specific autobiographical events are being recalled. However, it does not rely on the
specific mode of subjective experience accompanying the retrieval
of memory in the form of a first-person approach (Gardiner, 2001).
This other way of distinguishing episodic re-experiencing from
semantic familiarity has received relatively little attention in the
AM literature, despite the fact that Tulving’s conception of episodic
memory is inextricably bound up with the subjective phenomenological recollective experience.
It was to remedy this that we designed an original test,
known as the TEMPau task (Test Episodique de Mémoire du Passé
autobiographique, Piolino et al., 2000; for more details, Piolino,
Desgranges, Belliard, et al., 2003; Piolino et al., 2006), specifically to assess episodic AM, taking into account not only the
specificity of the personal events that are recalled (uniqueness,
spatiotemporal location, details), but also the subjective experience of remembering the encoding context. Episodic AM relies
not only on the ability to recall a specific event and locate it
in time and space, but also on the ability to recollect specific
details which distinguish that event from similar ones. As it is
possible to rebuild a specific event from one’s personal semantic
AM without actually reliving sensory–perceptual episodic details,
it is vital to gauge the specificity of details from the encoding
context through the sense of re-experiencing. The encoding context encompasses time and space (i.e. the specificity of event),
sensory–perceptual–affective–cognitive details (i.e. the specificity
of details), the subjective experience (i.e. autonoetic consciousness)
and the visual experience (i.e. self-perspective) (see Table 1).
Based on existing semi-structured questionnaires (Borrini et
al., 1989; Kopelman et al., 1989; Piolino, Desgranges, Benali,
& Eustache, 2002), the TEMPau’s originality lies in the way it
addresses the issue of the state of consciousness and the selfperspective accompanying memory retrieval across the entire
lifespan, by incorporating two kinds of subjective measures of
episodic re-experiencing (see Fig. 1). Participants are first given precise instructions to recall personal events from five different time
periods which occurred only once, at a particular place and date,
and lasted several minutes or hours but never more than a day. The
subjective reports of memories are then assessed using the Remember/Know procedure (Gardiner, 1988; Tulving, 1985), which makes
it possible to differentiate between episodic and semantic memory
retrieval, i.e. autonoetic consciousness from noetic consciousness.
An alternative response (“Guess”) is added in order to ensure that
the Know responses do not contain any degree of uncertainty,
compared with the Remember responses (Gardiner, Ramponi, &
Richardson-Klavehn, 1998). This Remember/Know/Guess procedure, originally used in the context of laboratory learning material
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
ARTICLE IN PRESS
4
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
Table 1
Operational criteria for assessment of episodic autobiographical memory.
Uniqueness
Short duration (less than 24 h)
Spatial situation
Temporal situation
Factual*
Spatiotemporal**
Phenomenological***
Specificity of event
Experimenter assessment of content
Specificity of details
Self-assessment of retrieval mode
Point of view (Field/Observer)
State of consciousness (Remember/Know)
Quality of memories
Field
Autonoetic
Vividness and number of visual mental images
Intensity and emotional valence
Frequency of rehearsal
Specific details that only belong to one particular event.
*
What, who, causes, circumstances.
**
Situation and sequence.
***
Perception, thinking, emotion.
such as wordlists, can be usefully applied to AM retrieval in conditions which tap more complex self-relevant information and the
long retention intervals inherent to real life. However, even today,
the Remember/Know procedure is seldom used to assess the state
of consciousness accompanying remote memories (e.g. Rybash &
Monaghan, 1999). Given that one feature of episodic memory is the
pulling together into a single episode of what, where, and when
something happened, the TEMPau test is designed to probe the different aspects of recollective experience, in particular the factual,
spatial and temporal features of memories. Thereafter, a procedure is used to check whether the R responses are infused with
the idiosyncratic perspectives, emotions and thoughts of the person doing the remembering. This procedure has previously been
carried out in laboratory studies in order to confirm that participants are obeying instructions when they give R responses
(see Gardiner, 2001). Besides autonoetic consciousness, the assessment of the rememberer’s self-perspective during autobiographical
recollection can be based on the viewpoint associated with the
Fig. 1. General organization of the TEMPau task (from Piolino et al., 2006). Description of the Test Episodique de Mémoire du Passé autobiographique (TEMPau) and recorded
scores. Method: The participants are asked to recall four specific autobiographical memories (or eight for the most recent time period) which have some relevance to their
personal lives, from five periods covering their entire lifespan (i.e. 0–17 years old (or childhood and adolescence), 18–30 years old (or young adulthood), more than 30 years
old except for the last 5 years (or older adulthood), the last 5 years except for the last 12 months (or relatively recent), the last 12 months (or very recent)). After recall,
spontaneous or otherwise, the participants are prompted up to three times to give more details if necessary and/or to be more specific if they have recalled a generic event.
After the recall of each event, whatever its level of specificity, the participants are required to report their self-perspective and state of consciousness during retrieval, before
the next cue is given (see Field/Observer and Remember/Know). In a field perspective, the participants keep the same viewpoint that they had in the original event, whereas
in an observer perspective, the participants see themselves in the event from the viewpoint of an external observer. During the state of consciousness task, separate responses
have to be given for the factual (what), spatial (where) and temporal (when) contents of memories. First, they select an Remember response if they can remember the specific
episode with its encoding context—in which case, they may virtually relive the previous event (e.g. details such as thoughts, feelings or images related to the recalled event),
a Know response if they just know this episode took place but cannot recall any specific event and cannot virtually relive any sensory or affective details pertaining to the
recalled event, or a Guess response if they just guess that they probably experienced this episode but neither remember nor know it. Thereafter, a procedure is used to check
each Remember response in terms of details (justified Remember). Scoring: Each event is scored on a 5-point episodic scale which takes into account the specificity of the
content (i.e. single or repeated event), the spatiotemporal situation, and more especially the presence of internal details (i.e. perceptions, thoughts, feelings). Two main total
scores are recorded per lifetime period examined: (a) an overall score called the AM score, which includes all the memories (both specific and generic) and corresponds to
the classic episodic memory score used in the Autobiographical Memory Interview (Kopelman et al., 1989) and (b) an episodic score, called the EM score which only includes
specific and detailed memories scoring 4. A spontaneity score is recorded on a 5-point scale that conversely takes into account the number of cues and/or prompts the
participant needed in order to recall a specific event instead of a generic one. The Field/Observer and Remember/Know paradigms and the justified Remember procedure
make it possible to record several further scores per period, i.e. the percentage of each type of response.
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
mental representations, known as the Field/Observer perspective
paradigm (Nigro & Neisser, 1983; Robinson & Swanson, 1993). In
total, episodic AM can be characterized as enabling someone to
“travel back in time” relive specific events and view these events
as they would originally have been seen through his or her own
eyes (see also Crawley & French, 2005).
According to Tulving’s ideas, justified Remember scores can be
regarded as coming closest to the notion of episodic re-experiencing
via autonoetic consciousness. Details in this case are deemed to
be episodic because they have been re-experienced. The TEMPau
task therefore proposes a stringent approach to testing episodic
AM retrieval across lifetime periods, based mainly on autonoetic
consciousness and self-in-time. The idea here is to consider how
participants recall matters just as much as what they recall (see
also Brewer, 1996; Conway & Pleydell-Pearce, 2000; Wilson & Ross,
2003).
3. New insights from the TEMPau task
3.1. Effects of age and time interval on episodic autobiographical
memory
Studies of AM across the lifespan have to deal with other factors that are intrinsically related to very long-term intervals, such
as the effects of age at encoding and age at retrieval, which can
blur the analyses of the effect of time interval per se. These factors
can be explored using assessment methods that make it possible to
evaluate the semantic and episodic components of autobiographical memory in subjects of different ages, by defining time intervals
so that retrieval can be studied with a fixed time interval whatever the subject’s age. Hence, if the boundaries of each time period
under consideration are defined according to the subject’s age, it
then becomes possible to differentiate between the effects of age,
retention interval and age at encoding. Accordingly, like Levine et
al. (2002), Piolino et al. (2002) used a semi-structured questionnaire (the precursor of the TEMPau task) to check that episodic
recall (i.e. specific and detailed memories) does indeed deteriorate with age and retention interval, whereas semantic recall (i.e.
general personal knowledge, such as the names of acquaintances,
addresses, jobs, etc.) is characterized by relative invariance. As far
as episodic memories are concerned, Piolino et al. (2002) observed
(1) the classic temporal distribution of memories (Rubin et al.,
1986; Rubin & Schulkind, 1997) characterized by a retention function covering a period of a few years and a clear recency effect,
together with (2) the existence of a significant reminiscence bump
in subjects of at least 50 years of age and (3) a period of childhood
amnesia. In this study, the average encoding ages for the reminiscence bump and childhood amnesia corresponded to 23 and
4 years respectively. The deleterious effects of age concerned the
retention function and the reminiscence bump, but not the period
of infantile amnesia. Further findings have been obtained more
recently using the TEMPau task. First, we demonstrated age effects
across all five lifetime periods on the specificity of event recall and
spontaneity of retrieval, as well as on the phenomenal experience
of remembering—i.e. self-perspective and the state of consciousness (Piolino et al., 2006). While the field perspective and sense
of remembering declined with age and remoteness, the sense of
just knowing and the observer perspective increased with age and
remoteness. These effects concerned the factual, spatial and temporal attributes of memories. These findings therefore suggest that the
ability to consciously recollect many specific events and relive the
context in which they occurred deteriorates with aging, in line with
the findings of classic laboratory tests (e.g., Clarys, Isingrini, & Gana,
2002; Perfect & Dasgupta, 1997; Parkin & Walter, 1992). In older
adults, the temporal distribution of Field and Remember responses
(justified or otherwise) provided for the temporal content of AM
5
was characterized by a recency effect and by an increase in these
responses for distant memories from the 18–30 years old period
(i.e. the reminiscence bump). Overall, the main findings highlighted
the fact that aging and remoteness not only affect the specificity of
details, but also autonoetic consciousness and the self-perspective.
The evidence of contrasting temporal profiles for the Field/Observer
responses, mirroring the result for the Remember/Know responses,
supports the view that there is a shift in the phenomenal experience
of remembering real-world events with the passage of time that
causes a “Remember-to-Know” and “Field-to-Observer” shift over
time (Cermak, 1984; Conway et al., 1997; Linton, 1986). The greatest “Remember-to-Know” shift concerns the temporal attributes
of AMs. However, although episodic AMs decrease with age and
remoteness, some of them resist because there are self-relevant
(e.g. self-defining memories, Conway et al., 2004) and therefore
continue to retain the same main features as before, regardless of
the person’s age (i.e., mental reliving of affective and perceptual
details, accessibility, and self-perspectives). Interestingly, we found
that age had a gradual effect on the ability to justify Remember
responses by recalling specific details, whatever the period and irrespective of the content, although this ability was better preserved
for remote time periods than for more recent ones. Therefore, subjective episodic re-experiencing in the form of travelling back in
time to relive personal events is more objectively preserved in the
most distant past than in the recent past, which may explain why
elderly subjects often think their remote memories are better preserved than more recent ones.
Continuing on the theme of the superimposition of subjects’
age and the age of their memories, the effect of age at encoding
on the recall of the most remote period of life covering the childhood and early adolescence has been further explored using an
adaptation of the TEMPau task aimed at school-age children aged
from 6 to 13 years (Piolino, Hisland, Matuszewski, Jambaqué, &
Eustache, 2007). This study highlighted age-related differences in
episodic AM, whereas personal semantic memory (based on general knowledge, such as the names of familiar people or heroes,
personal and school addresses, and lessons at school) was characterized by relative developmental invariance. This profile paralleled
the developmental dissociation revealed by the Remember/Know
paradigm, i.e. autonoetic/noetic consciousness. Increasing age was
particularly important in the spontaneity of recall and number of
“Remember” responses and their justification in terms of the actual
contextual details that were retrieved—factual, spatial and, more
especially, temporal details. These findings support the view that
mental time travel through subjective time, which allows one to
re-experience the past through self-awareness, is one of the last
features of autobiographical memory to become fully operational.
This is in keeping with Tulving’s theory (1985, 2001, 2002) that
episodic memory develops later in ontogeny than semantic memory. This assumption has been considered in light of the theory of
infantile amnesia originally defined by Freud (1905). According to
this, adults are unable to subjectively re-experience the circumstances of early personal events encoded before the age of 5, not
because of a problem of retrieval, but because of the absence of
truly episodic memory before that age (Wheeler et al., 1997; see
also Nelson & Fivush, 2004).
Research carried out more recently in our laboratory has highlighted the role of executive functions in the generative retrieval
mechanisms involved in the emergence or impairment of episodic
AM retrieval in children or older adults (Piolino, Desgranges, &
Eustache, 2008). Moreover, different factors other than age and
remoteness, such as emotion and images of the self, are important to study as they are indeed also crucial to AM retrieval in
healthy subjects (Libby & Eibach, 2002; Talarico, Labar, & Rubin,
2004) as in patients (see Conway et al., 2004; Guillery et al., 2000;
Noël et al., 2008; Williams et al., 2007). For example, while we con-
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
6
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
firmed in patients with depression a diminution in episodic AMs
(i.e. specificity of details, autonoetic consciousness and field selfperspective) compared to healthy controls, all the more concerning
positive events (Lemogne et al., 2006), we observed in healthy
young adults a relationship between a diminution in episodic AMs
(i.e. specificity of details, autonoetic consciousness and field selfperspective), and the cognitive avoidance of intrusive emotional
recollections (Lemogne et al., 2009).
3.2. Neural substrates of the re-experiencing of episodic
autobiographical memory over time in normal subjects
We have discovered that some relevant episodic AM persist
regardless of the time periods being considered, even in older
adults. We investigated the neural substrates of these episodic
AMs by adopting two complementary approaches, namely activation studies in normal adults and correlational studies between the
TEMPau task and resting-state neuroimaging measures.
Yet a great many functional neuroimaging studies have explored
the activation triggered by AM tasks in healthy subjects (for reviews,
see Cabeza & St Jacques, 2007; Conway, Pleydell-Pearce, Whitecross,
& Sharpe, 2002; Maguire, 2001; Svoboda, McKinnon, & Levine,
2006). They have found evidence of a large network encompassing the prefrontal, medial and lateral temporal cortices, as well
as posterior regions, but yielded controversial results concerning
the relationship between the MTL structures and the length of
the retention interval. Some studies (e.g. Maguire & Frith, 2003a;
Niki & Luo, 2002; Piefke, Weiss, Zilles, Markowitsch, & Fink, 2003)
have reported differing degrees of engagement of the hippocampal region in recent and remote AM retrieval, seemingly arguing
in favour of the standard model of memory consolidation. Others
have provided evidence that semantic memory retrieval involves
the MTL regardless of remoteness, which is problematic for the two
conflicting theories (Bernard et al., 2004). Most of the other studies
failed to find any differential involvement of the MTL as a function of
time interval (for reviews, see Cabeza & St Jacques, 2007; Svoboda et
al., 2006), thereby contradicting Standard Theory predictions and
supporting Multiple Trace Theory ones instead. In some of these
studies, methodological confounds may have biased certain results.
For instance, in most cases, a questionnaire was administered a few
weeks or days prior to the scanning session in order to obtain material for constructing the cues used during scanning to reactivate
old memory traces. Only a few studies tried to prevent subjects
from reencoding their memories via the hippocampus (e.g. Gilboa,
Winocur, Grady, Hevenor, & Moscovitch, 2004; Okuda et al., 2003).
In our set of studies, we designed specific protocols based on
the TEMPau paradigm in order to capture the neural correlates of
episodic AM recollection fulfilling five main principles: (1) avoiding the reencoding of memories prior to the scan; (2) promoting the
retrieval mode of episodic AM through re-experiencing; (3) probing different lifetime periods; (4) taking into account the dynamics
of AM retrieval; and (5) controlling for the episodic nature of memories that are retrieved and the qualities of recollection.
In an initial Positron Emission Tomography (PET) activation
study of young adults (Piolino et al., 2004), we examined the mental retrieval of recent (last 12 months) and remote (5–10 years ago)
episodic AMs from sentence cues (e.g. a party with your friends
within the last year or a special party with your friends that took
place when you were between 17 and 20 years of age) controlling
for memory access time. The sentence cues were selected from a
previous experimental study of AM in healthy subjects on the basis
of their likelihood of producing specific detailed AMs in young subjects with the same ease of access regardless of time interval. Prior
to scans, the subjects were trained to mentally relive episodic AMs
(different from the scanning) with as many episodic details as they
could, such as time, location, perceptions and feelings, when they
Fig. 2. The percentage of justified Remember responses (mean %) as a function of
age group in school-age children (top) and adults (bottom) for each lifetime period
(adapted from Piolino et al., 2006; Piolino, Hisland, Matuszewski, et al., 2007).
listened to the sentence cues. After the scans, they were asked to
retrieve these evocations again, but this time out loud. The nature
of the AMs they retrieved was assessed according to objective measures performed by the experimenters (i.e. specificity and details),
as well as to more subjective measures performed by the subjects
themselves, regarding the retrieval strategy they had used (verbal
or visual), frequency of rehearsal (from none to very frequent), state
of consciousness (Knowing or Remembering), vividness of mental
visual imagery (from vague to very clear), self-perspective (Field
or Observer) and emotion (from none to very intense at encoding
or retrieval). The main finding was that the retrieval of both recent
and remote episodic AMs was characterized by specificity, autonoetic consciousness, visual imagery and emotion, and principally
activated a widespread left-sided network (i.e. left prefrontal, temporal and parietal, anterior cingulate cortex, left fusiform gyrus, left
subcortical areas), plus the bilateral posterior cingulate cortex and
cerebellum and the bilateral hippocampus. Interestingly, the findings pointed to greater hippocampal activity for remote memories
than for recent ones and a predominantly right-sided hippocampal involvement, whatever the remoteness of the autobiographical
memories. (Fig. 2).
The second study was designed to explore memories from
across the lifespan of older healthy subjects aged approximately
70 years (Viard et al., 2007) and therefore to conduct brain measures of AM recollection for very long retention intervals, lasting
decades. The five main principles were the same as before, but
we adopted another method of selecting sentence cues and used
functional Magnetic Resonance Imaging (fMRI) instead of PET. This
time, we asked husbands to describe specific relevant events from
their wives’ lives, covering the same five time periods as those
in the TEMPau task. We were thus able to identify the brain
structures involved in the recollection of episodic AMs across the
whole lifespan from personally relevant cues, selected by question-
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
7
Fig. 3. Images showing results of the small volume correction analysis centred on the hippocampus. Coronal planes indicate left hippocampal activation for P1 (0–17 years
old) and P5 (last 12 months) and bilateral hippocampal activation for P2 (18–30 years old), P3 (more than 30 years old), and P4 (last 5 years). Colour scale: voxel Z-score values
(from Viard et al., 2007).
ing a family member. The findings showed that the recollection
of episodic AMs from the five time periods triggered activation
within a circumscribed network, including the left hippocampus
and superior frontal gyrus, as well as the bilateral precuneus and
posterior cingulate gyrus. In addition, the period of the reminiscence bump showed specific activation in the left lateral temporal
lobe. Behavioural results indicated that, regardless of the age of
the memories, recollection was characterized by specificity (i.e.
spatiotemporal uniqueness and details), as well as by an autonoetic state of consciousness and mental visual imagery, attesting
to their episodic nature. However, remote memories from young
and older adulthood periods (18–30 years old and more than 30),
as well as from the last 5 years, were rated more strongly in terms
of phenomenological characteristics (emotional intensity, image
quality or autonoetic consciousness) than those from both the most
remote and most recent periods. These three time periods also
triggered the activation of the right hippocampus (Fig. 3). Regardless of the time periods, both anterior and posterior parts of the
hippocampus were activated (see Lepage, Habib, & Tulving, 1998;
for a discussion on the functional distinction between the anterior
and posterior hippocampus in terms of encoding and retrieval processes). New analyses of connectivity between the hippocampus
and neocortex have highlighted significant correlations between
the activation of the MTL and the activation of the neocortical
regions for both recent and remote periods, albeit to a lesser extent
for the most recent period (Viard et al., submitted). Interestingly,
the latter pattern of results highlighted a bilateral network concerned with episodic AM retrieval. More specially, from the distant
past, bilateral hippocampal activation was predicted by other MTL
structures (parahippocampal gyrus and amygdala) and by the neocortical regions (lateral temporal cortex and temporal pole).
As a follow-up to our PET activation study, we used
another powerful approach—the cognitive–metabolic correlative
technique—which requires both cognitive tests and resting-state
PET scans to be conducted within a short time interval (a few days at
most), and correlations to be performed between these two sets of
data across a group of subjects. PET makes it possible to study physiological parameters such as blood flow or metabolism, which are
closely related to synaptic activity. It is a well-validated method for
mapping the functional neuroanatomy of a given behaviour in neu-
rodegenerative diseases (Desgranges et al., 1998; Desgranges et al.,
2002; Eustache, Desgranges, Giffard, de la Sayette, & Baron, 2001;
Rauchs et al., 2007; Teipel et al., 2006; see Salmon, Lekeu, Bastin,
Garraux, & Collette, 2008, for review). It is particularly useful for
establishing cognitive and neurobiological models of human memory, because it allows the mapping of cerebral networks subserving
a particular task and can be used to identify regions whose involvement is crucial to the task (see Tulving, Habib, Nyberg, Lepage,
& McIntosh, 1999; for a discussion of the concepts of “how sites”
and “what sites”). More relevant to the present discussion, the correlative method offers an alternative approach which overcomes
some of the methodological limitations to AM neuroimaging studies (e.g. no direct control over the nature of episodic AM activated
inside the scanner, the intrinsic difficulty of disentangling reencoding processes from retrieval ones and recall of abstract semantic
knowledge from that of specific information) enabling the use of
sophisticated cognitive assessments where the nature of memories
can be strictly controlled.
The adoption of a cognitive–metabolic approach in order to
reveal the neural substrates of AM in healthy subjects was justified
by the variability of both cognitive AM performances (Levine et al.,
2002; Piolino et al., 2002; Piolino et al., 2006) and brain functions
(Coles et al., 2006). This approach is particularly suitable for healthy
middle-aged and elderly subjects, who present greater intersubject
variability than young subjects (Piefke & Fink, 2005).
The aim of our neuroimaging study of healthy subjects was to
pinpoint the brain structures whose synaptic function subserves
the recollection of lifetime episodic AM, establishing correlations
between resting regional Cerebral Blood Flow (rCBF) measured
with PET and AM indexes regarding rich episodicity (i.e. the recollection of specific events with episodic details corresponding to
justified Remember responses) and spontaneity (i.e. the retrieval of
memories without retrieval support) obtained separately using the
TEMPau task (Piolino et al., 2008). The results of 12 healthy middleaged subjects showed that the majority of memories involved a
field perspective, gave rise to a sense of remembering which was
justified in terms of specificity and details, and were relatively
spontaneously retrieved, regardless of their remoteness. Based on a
priori hypotheses regarding the involvement of the frontotemporal
neocortical structures and hippocampal region in AM retrieval (see
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
8
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
Cabeza & St Jacques, 2007; Conway et al., 2002), we first extracted
the mean rCBF for each anatomical volume of interest selected
from a bilateral set of regions of interest covering the left and right
frontal and temporal lobes. Our paradigm gave us the opportunity to single out two distinct aspects of AM retrieval, by recording
the generative processes (i.e. spontaneity index) and the recollection based on autonoetic consciousness with reliving of episodic
details (i.e. episodicity index). The main results indicated that the
rCBF values for the right hippocampus predicted the episodicity
index (unlike the index of semantization, based on Know memories) regardless of the content (but spatial > factual > temporal
details) and age of the memories, while that of the left medial
orbital frontal gyrus predicted the index of spontaneity, again for
every lifetime period. Second, a voxel-based analysis of the whole
brain using an exploratory approach confirmed these striking relationships between episodic AM and rCBF in the medial temporal
regions, including the hippocampus, and between the spontaneity
of access to specific memories and rCBF in the frontal regions (see
Fig. 4A1 and A2). Other correlations for the episodicity index concerned a network which bilaterally encompassed the hippocampus,
parahippocampus, precuneus, lingual gyri and thalamus, regardless
of the period, with additional involvement of temporal and prefrontal neocortical regions for some of these periods. Concerning
the spontaneity index, the main correlations concerned the prefrontal cortex bilaterally, more specifically the orbitomedial surface
(ventromedial part of Brodmann Area 10; medial parts of BA 11
and 47). Further SPM results (Fig. 5) showed that the field perspective was mainly correlated with the right MTL (hippocampus and
parahippocampus) and lingual gyrus and left temporal pole, while
observer memories were mainly correlated with the left dorsolateral and superior frontal gyri and bilateral posterior areas (cuneus
and occipital lobe).
Overall, these findings for healthy subjects emphasize the notion
that the hippocampus and neocortical regions are permanently
involved in episodic AM retrieval, regardless of remoteness. Rightsided or bilateral involvement of the hippocampus characterizes
rich episodic AM recollection (see Section 4).
3.3. Neural substrates of the re-experiencing of episodic
autobiographical memory over time in brain-damaged patients
Some memory diseases have a massive impact on AM, especially
its episodic subcomponent (for reviews, see Conway & Fthenaki,
2000; Kopelman, 2000; Kopelman & Kapur, 2001). Studies of lesions
in non-demented patients have emphasized the role of frontotem-
Fig. 4. SPM T-maps of significant correlations between TEMPau scores and resting
brain measures (PET) for three lifetime periods. (adapted from Eustache et al., 2004
(B); Piolino, Chételat, Matuszewski, et al., 2007 (C); Piolino, Desgranges, Hubert,
et al., 2008 (A1 and A2))—(A1 and A2). Results in normal middle-aged subjects
for the correlation between cerebral blood flow (CBF) and the episodicity (based
on autonoetic consciousness) and spontaneity indices (p < .005 uncorrected, cluster
size k > 100)—(A1 and A2). Results in early to moderate Alzheimer’s disease (AD) for
correlation between FDG uptake and the AM index (p < .01 uncorrected, cluster size
k > 80)—(B). Results in frontotemporal dementia (FTD) for correlation between FDG
uptake and the AM index (p < .005 uncorrected, cluster size k > 100)-(C).
Fig. 5. SPM T-maps of significant correlations between self-perspective in the TEMPau task and resting brain CBF measures (PET): field (in the left) and observer (in the right)
viewpoints in healthy elderly subjects (p < .005 uncorrected, cluster size k > 100).
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
9
Fig. 6. SPM T-maps showing the significant hypometabolism found in Patient CL compared to normal controls (PET-FDG, p < 0.001 uncorrected) projected in transverse
position and TEMPau CL’s performances (adapted from Piolino et al., 2005). Caption: Detailed scoring for each of the post-onset memories (no pre-onset memories) recalled
by CL in the TEMPau task (from the last12-month-period, and Christmas and summer 1997 from the last 5-year-period) using a fine-grained 6 half-point episodic scale,
shown alongside controls’ results (mean rating scores), from the shortest interval (today) to the most distant interval tested, and CL’s subjective Remember, Know or Guess
responses accompanying each of his recollections. Data shown are the mean rating scores for controls from each question tested on the patient. CL’s raw scores are shown
with statistical significance according to Z-scores (pathological score: ** p < 0.01; *** p < 0.001).
poral areas in AM disruption, especially the right side (for reviews,
see Markowitsch, 1995; Kopelman, 2000). For example, Patient
ML (Levine et al., 1998) suffered from organic focal retrograde
amnesia after a head injury resulting in right-sided frontal damage (BA 47) that involved the uncinate fasciculus and may have
disconnected the frontal and temporal structures. Using the TEMPau task, the right prefrontal cortex was also found to be involved
in a case study of disproportionate retrograde amnesia (Piolino
et al., 2005). Patient CL manifested a sudden and persistent total
loss of personal identity in the context of clinically documented
good everyday memory and normal neuroanatomical data (CT scan,
MRI). When compared with an age-matched control group, the
hypometabolism was found to be entirely restricted to the right
orbitofrontal cortex (BA 11/47, Fig. 6). CL’s state of mind was “a
blank” whenever he tried to think about his past. Even his postonset episodic AMs were fragile: he retained a subjective sense
of remembering for the last few days and weeks, but was unable
to recollect more distant personal events through mental time
travel, even those that were particularly self-relevant (e.g. his “first”
Christmas).
The mechanisms by which episodic AM retrieval is disrupted
and their connection with the frontotemporal structures have
also been studied in demented patients with cortical dysfunction.
Our neuropsychological data revealed strongly contrasting profiles
of autobiographical retrograde amnesia according to the type of
dementia (Piolino, Desgranges, et al., 2003), in keeping with other
studies (e.g., Ivaniou et al., 2006; Nestor, Graham, Bozeat, Simons,
& Hodges, 2002). More specifically, in Alzheimer’s disease, which
preferentially affects the medial temporal lobe in the early stage of
dementia, we observed temporally graded memory deficits obeying Ribot’s Law, with remote memories being better preserved than
recent ones. Nevertheless, a fine-grained analysis showed that rel-
atively preserved remote memories in Alzheimer’s disease were,
in fact, semanticized memories, with the result that episodic AM
had an entirely flat gradient. In semantic dementia, characterized
by mainly external temporal lobe lesions with relative sparing of
the medial temporal lobe, our data revealed memory loss with a
reverse gradient. However, an assessment based on a sense of recollection (Remember responses) unconstrained by verbal abilities
brought to light a relative preservation of episodic AM in early-stage
semantic dementia, regardless of the lifetime period (see also Moss
et al., 2000; Piolino, Belliard, Desgranges, Perron, & Eustache, 2003;
Westmacott et al., 2001 for similar findings). Lastly, in the frontal
variant of frontotemporal dementia, results showed memory loss
without any clear temporal gradient (see also Matuszewski et al.,
2006). Episodic memories in their strictest definition (i.e., unique,
detailed, specific in time and space) were impaired, whatever the
time interval considered in the three groups, though memory loss
was global in Alzheimer’s disease and frontotemporal dementia,
and temporally graded in semantic dementia, sparing the most
recent period. These results demonstrate that autobiographical
amnesia varies according to the nature of the memories under consideration and the locus of cerebral dysfunction. We have discussed
these profiles of autobiographical amnesia in the light of the two
competing models of long-term memory consolidation and recent
conceptions of autobiographical recollection (Piolino, Desgranges,
et al., 2003). Principally, the existence of a temporal gradient for
semanticized AM but total episodic retrograde amnesia (regardless
of the period) resulting from MTL damage in early Alzheimer’s disease supports the Multiple Trace Theory rather than the Standard
Theory.
The main objective in conducting a series of neuroimaging studies in neurodegenerative diseases was to further unravel the neural
bases of clear-cut temporal gradients in AM deficits, according to
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
10
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
the type of dementia. We used the same approach as we had done
in the healthy elderly adults, looking for correlations between the
resting-state cerebral measure and temporally graded AM scores
in order to identify the brain structures whose synaptic dysfunction subserved the impairment. To this end, we studied a group
of 17 Alzheimer’s disease patients with mild to moderate dementia (Eustache et al., 2004). We administered an abridged version of
the TEMPau task, assessing just three broad time periods (childhood and teenage years (0–17 years old), middle age (more than
30 years old) and the previous 5 years), and measured resting
cerebral metabolic rate of glucose using PET (resting normalized
fluorodeoxyglucose uptake). The findings showed diverse correlation patterns according to the time period being tested: the
correlations were restricted to the left middle frontal gyrus for
the teenage and childhood period, the bilateral prefrontal cortex
(bilateral superior, bilateral middle and right inferior gyri) for the
middle-age period, and the right hippocampus and right frontal and
temporal gyri for the last 5 years (see Fig. 4B). The data showed that
the hippocampus became disengaged from the retrieval of remote
AMs, which became semantic instead of episodic. These findings are
consistent with both models of memory consolidation, in that the
latter share the notion of the temporary role of the hippocampus in
semanticized memories. In the same vein, the shift from right to left
frontal regions as the time interval increases may reflect the move
away from an episodic retrieval mode towards a more semantic one
(see Hemispheric Encoding/Retrieval Asymnetry model, Tulving,
Kapur, Craik, Moscovitch, & Houle, 1994).
In order to examine the specificity of the neural bases of AM
impairments depending on the type of neurodegenerative disease,
we applied the same methodology, this time examining 5 lifetime
periods, to a group of 20 patients with frontotemporal dementia (Piolino, Chételat, Matuszewski, et al., 2007). Behaviourally,
the frontotemporal dementia patients’ performances were relatively similar to those of the Alzheimer’s disease patients, in
that they provided generic memories instead of event-specific
sensory–perceptual–affective details, but without the temporal
gradient, and displayed deficits in the sense of reliving and
self-perspective during retrieval (i.e. providing more Know and
Observer responses). This pattern was very similar to that found
in a group of patients with traumatic brain injury, who manifested
deficits in specificity, autonoetic consciousness and field perspective across all the lifetime periods (Piolino, Desgranges, Manning, et
al., 2007). The investigation of the mechanisms responsible for AM
deficits in frontotemporal dementia related not only to executive
functions, as in our traumatic brain injury group, but also to semantic verbal skills, as in semantic dementia patients (see Matuszewski
et al., in press). The cognitive–metabolic correlations in frontotemporal dementia (Fig. 4C) revealed that the AM deficits stemmed
mainly from the dysfunction of the left-sided orbitofrontal regions
(BA 11) and, to a lesser extent, that of the left-sided dorsolateral
(BA 6), frontal and temporal neocortical regions, whatever the time
period. Additional analysis showed that deficits in specific memories were correlated with a dysfunction of the left orbitofrontal
areas, whereas the impaired production of generic memories was
correlated with a dysfunction of the left temporal pole.
We were therefore able to confirm the existence of a specific
pattern of correlations in frontotemporal dementia compared with
Alzheimer’s disease, highlighting the effectiveness of the correlative approach in shedding light on the mechanisms underpinning
different profiles of AM deficits. More specifically, the mechanisms
of deficits in Alzheimer’s disease (characterized by a temporal gradient) were found to involve the hippocampus for recent AMs
(i.e. mainly anterograde memories) and the prefrontal cortex for
remote ones. By contrast, our findings support the view that AM
deficits in frontotemporal dementia (characterized by a flat gradient) mainly stem from orbital prefrontal and lateral temporal
dysfunction, regardless of the time period. The pattern of correlations therefore underlines the similarity of the mechanisms behind
deficits in anterograde and retrograde memories in frontotemporal
dementia, unlike Alzheimer’s disease.
Overall, these studies yielded arguments in favour of the role of
the MTL, and more specifically the hippocampus, in the retrieval of
recent and remote episodic AMs, unlike the retrieval of semantic
AM, in keeping with the Multiple Trace Theory. We attempted to
find further arguments for Multiple Trace Theory in non-demented
patients with focal lesions within the MTL. Neuropsychological
investigations designed to examine the extent of retrograde AM
deficit in unilateral MTL lesions, be they single-case or group studies, have proved controversial, especially regarding episodic AM.
In collaboration with a research group specializing in epileptic
patients (Noulhiane, Piolino, Hasboun, Baulac, & Samson, 2007;
Noulhiane, Piolino, Hasboun, Baulac, & Samson, 2008), we carried
out a study of 22 patients who had undergone a left- (n = 12) or
right-sided (n = 10) MTL resection for the relief of epileptic seizures,
using a correlative approach based on the TEMPau and precise MRI
volumetric measures of the remaining tissue of the temporal lobe,
including different regions of the MTL (i.e. hippocampus, entorhinal, perirhinal and parahippocampal cortices), temporopolar, and
the lateral temporal lobe (i.e. superior, middle and inferior temporal gyri). Both patient groups displayed impaired episodic AM
retrieval across all time periods, compared with matched control
subjects, reflecting particular difficulty in producing specific and
detailed memories, associated with poor autonoetic consciousness,
as revealed by the small number of justified Remember responses
across all periods. This result was in keeping with some other recent
studies, which have shown that the famous Patient HM (Steinvorth et al., 2005) who underwent bilateral MTL removal to control
intractable epilepsy (Scoville & Milner, 1957), and groups of patients
with either right or left MTL damage (Viskontas, McAndrews, &
Moscovitch, 2000) were in fact equally deficient in episodic AM
across their entire lifespan, without any temporal gradient, whereas
personal semantic and generic memories were spared. That said,
we noticed that the patients with a right-sided resection had more
difficulty in recollecting episodic details from the reminiscence
bump period (18–30 years old), whereas the patients with the leftsided resection experienced particular difficulty regarding the most
recent period. Analyses of correlations between MRI volume measures of temporal lobe structures and autobiographical memory
scores showed that there was no such correlation with the volumes
of the lateral temporal lobe structures, but revealed that right MTL
structures predicted episodic AM scores regardless of remoteness.
Therefore, these findings confirmed the permanent role of MTL in
episodic AM retrieval in keeping with the Multiple Trace Theory.
3.4. Deficits in the re-experiencing of episodic autobiographical
memory through time travel and the sense of self
As AM provides knowledge of one’s experiences across time,
enabling the integration of past and present selves, AM deficits predict a weakened sense of self (Bluck, 2003; Conway et al., 2004).
However, it can be noted in our AM studies that age-related deficits
in AM fail to weaken self-coherence in healthy elderly participants (Duval, Eustache, & Piolino, 2007) as opposed to our patients
with psychiatric diseases such as depression (Lemogne et al., 2006)
and schizophrenia (Danion et al., 2005), and neurological diseases
such as Alzheimer’s Disease, or frontal lobe damage who present
severe retrograde amnesia with loss of self-identity. One of our
studies (Piolino et al., 2006) has provided further evidence that,
despite episodic AM deficits in aging, the preservation of (a) personal semantic memory, which is a fundamental component of
personal identity (Conway et al., 2004; Tulving, 1993; Wilson &
Ross, 2003), (b) the subjective sense of remembering for the remote
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
past, and (c) some episodic memories, enables healthy older people
to “travel back into their past”, thereby ensuring a sense of identity
and continuity in time.
We also observed that patients with frontal lobe damage or
medial temporal lobe damage had a selective deficit in episodic AM,
with relative preservation of semantic AM, and an impoverished
ability to consciously recollect their past, even though they knew
about their past, giving a clear example of the distinction between
autonoetic remembering and noetic knowing. The reverse dissociation has been described in rare cases of patients with early-stage
semantic dementia, who lose some personal semantic knowledge
but are still able to recollect some episodic details (Piolino, Belliard,
et al., 2003). More generally, our patients with episodic AM disruption presented deficits in specificity, autonoetic consciousness and
self-perspective, and were hampered in their ability to “travel back
in time”, relive specific events and view these events as they would
originally have been seen through their own eyes. Like Patient KC,
they still had a sense of personal identity, in that they could answer
the question “Who am I?”: they knew their name, those of family, friends and colleagues, some general information such as that
given in a curriculum vitae, and also repeated personal events.
However, they were frequently unable to recollect the slightest specific personal event, even the most relevant and emotional ones.
Depending on the extent of the episodic AM disruption, their personal identity was more or less devoid of “intimacy”, which has
been regarded as one of the main phenomenological properties of
recollection since James (1890). With the progression of dementia
and the additional impairment of semantic AM, deficits eventually
extended to a loss of conceptual self (see Addis & Tippet, 2004).
This observation is significant at two levels: first, it clearly confirms a dissociation in autobiographical memory between episodic
and semantic aspects, and secondly, it clearly demonstrates that
personal identity does not only involve conceptual self-knowledge
(Conway et al., 2004), but also relies on episodic attributes, such
as autonoetic consciousness, which allow individuals to remember
the past in an experiential way. Indeed, one of the main functions
of episodic AM is not only to adapt itself to the present but also to
maintain continuity of self in subjective time. It is the phenomenological self that gives us the ability to remember specific instances
which illustrate why and how we know who we are.
4. General discussion
We conducted a series of studies of episodic memory based on
a special method for assessing episodic AM across lifetime periods which placed the emphasis on the central attribute of episodic
memory, namely the autonoetic re-experiencing of past events
via subjective mental time travel. With regard to the neural substrates of episodic AM over time, these studies broadly highlighted
the cerebral network that was recently identified in the review
by Cabeza & St Jacques (2007). More specifically, they clarify the
network’s role in different aspects of re-experiencing AM through
mental time travel and its links with other cognitive functions. We
begin by discussing the convergent evidence for the constructive
and dynamic nature of episodic AM over time, emphasizing the
role of prefrontal and external temporal regions. We then go on to
evoke the role of the MTL, and more especially the hippocampus,
in episodic AM retrieval, focusing on changes over time and the
phenomenological attributes.
4.1. The constructive and dynamic nature of episodic AM across
time
Our cognitive findings in children and elderly subjects and
our neuropsychological and neuroimaging findings clearly confirm that the episodic and semantic subcomponents of AM can
11
be dissociated, but are also closely linked, at both cognitive and
neural levels; they have common and unique processes. This is in
line with neuroimaging studies that have emphasized betweensystems similarities and within-system differences during episodic
memory and semantic memory (Burianova & Grady, 2007; Levine
et al., 2004; Nyberg, Forkstam, Petersson, Cabeza, & Ingvar, 2002).
More specifically, our developmental outcomes (in children and
elderly subjects alike) confirm that episodic memory is a “latedeveloping, and early-deteriorating past-oriented memory system,
more vulnerable than other memory systems to neuronal dysfunction” (Tulving, 2002, p. 5).
Furthermore, the study of the cognitive mechanisms behind
episodic AM disruption has provided evidence in support of
the multifaceted nature of episodic AM retrieval and construction, which calls on multiple processes: gaining access
to sensory–perceptual–cognitive–affective specific details elicits
visual imagery and the autonoetic experience of mentally “reliving” a unique past event, and involves executive processes which
interact with personal semantic knowledge. Accordingly, the neuropsychological data of patients with frontotemporal dementia
or semantic dementia clearly show that AM disruption stems
from a deficit in the generative/construction processes that trigger episodic AMs, processes which are closely linked to executive
and semantic functions subtended by frontal and anterior temporal
regions (Conway & Fthenaki, 2000; Conway et al., 2002).
Otherwise, neuroimaging studies of healthy subjects have
revealed that the recollection of episodic AMs associated with a
sense of remembering requires retrieval processes that are reliant
on the prefrontal cortex and lateral temporal lobe for generative
and semantic processes, but also on the medial temporal lobe for
recollection (autonoesis, emotion, self-perspective), and parietooccipital regions such as the cuneus/precuneus for mental visual
imagery. The data suggest that episodic AMs are triggered in the
prefrontal cortex and generated through information stored in networks located near the posterior brain via the hippocampus, which
plays a special role in recollecting and binding all the multifaceted
attributes of episodic AM (e.g. images, feelings, see below). This is in
keeping with neuropsychological studies that have shown that AM
is disrupted by frontal and/or temporal lobe lesions (see Conway
& Fthenaki, 2000; Kopelman & Kapur, 2001; Markowitsch, 1995,
for reviews), by more posterior lesions (Greenberg & Rubin, 2003)
or by their disconnection (Levine et al., 1998; Piolino et al., 2005).
At the cognitive level, breakdowns in executive function, but also in
episodic and semantic memory, can play a major role in episodic AM
disruption, as comprehensively illustrated by the contrasting patterns of autobiographical amnesia in the three neurodegenerative
diseases we explored.
We also found that specificity, the subjective sense of remembering and the original field perspective, all of which are deemed
to be critical features of episodic memory, are prone to fading and
decay over time. However, even if the semantization of episodic
memories over time does indeed occur, some lifelong episodic
AMs resist this trend. At the neural level, we found that semanticized AMs ceased to depend upon the MTL (i.e. in studies of
healthy subjects and Alzheimer’s disease patients), while episodic
AMs remain under the influence of the MTL and MTL-neocortical
links. Of particular interest, we noted the presence of external
temporal lobe activation or correlation, clearly demonstrating the
increasing role of semantic processes in episodic AM retrieval over
time and, more generally, the dynamic relationships between both
subcomponents of AM. For example, the 18–30 years old period,
which concerns the reminiscence bump, containing vivid and selfrelevant phenomenological episodic memories, was characterized
by the additional involvement of the right superior temporal pole
and superior/middle temporal gyrus. This period includes events
encoded during adolescence and young adulthood which are par-
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
12
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
ticularly well-remembered by subjects over 40 years old and are
relatively well-protected from the deleterious effects of time and
age (Piolino et al., 2002; Piolino et al., 2006). Hence, this result
stresses the role of semantic knowledge in accessing episodic memories from the reminiscence bump which are particularly critical to
one’s sense of identity (Conway & Pleydell-Pearce, 2000; Fitzgerald,
1996). Leaving aside the reminiscence bump, the temporal pole and
lateral temporal regions correlated with MTL regions and episodic
re-experiencing during the retrieval of recent and remote periods
alike. The role of both external temporal regions in episodic AM
is consistent with the fact that lesions to the temporopolar region
may cause focal retrograde autobiographical amnesia (Wheeler &
McMillan, 2001) as this region is deemed to act as a convergence
zone, binding information from the hippocampal structures and
posterior association regions (Damasio, 1989; Markowitsch, 1995).
Moreover, there is evidence to link the functions of the lateral
temporal lobes and temporal pole to personal semantic memory
processes (for a review, see Svoboda et al., 2006). Lastly, we were
able to demonstrate that the percentage of generic memories provided by frontotemporal dementia patients was correlated with the
metabolism of the left temporal pole. Overall, our findings substantiate the notion that executive and both episodic and semantic
memory processes are integral parts of episodic AM recollection,
because of their special role they play in constructing an AM trace
(Conway et al., 2002; Levine et al., 2004; Svoboda et al., 2006).
Therefore, episodic AM studies make it possible to look at
episodic memory representations and processes from a much more
dynamic perspective than the recall of stimuli presented in the
laboratory. Several studies have demonstrated that the conscious
recollection of autobiographical events involves common but also
unique processes compared with this kind of recall (Nyberg et al.,
2002; Burianova and Grady, 2007). Our studies were specifically
designed to enlight the evolution and reorganization of personal
experiences over the course of time and to unravel the complex
mechanisms of episodic AM retrieval pinpointing the role of the
frontal and medial temporal structures in these mechanisms.
4.2. The role of left prefrontal regions in episodic AM retrieval
As far as the role of the prefrontal cortex and executive functions
in episodic AM retrieval deficits is concerned, our neuropsychological and neuroimaging examinations of frontotemporal dementia
and traumatic brain injury patients (as well as normal elderly
subjects) provide rigorous convergent evidence, regardless of the
lifetime period. This is in line with the literature on autobiographical amnesia in patients with focal lesions to the frontal lobe and
the findings of neuroimaging studies of normal subjects, which have
shown that the frontal lobe plays a crucial role in episodic memory and autonoetic consciousness (Wheeler & Stuss, 2003; Wheeler
et al., 1997). These data are not only consistent with the role of
the prefrontal cortex in self-referential processes, but also with its
role as a working-with-memory structure that is involved in strategic aspects of retrieval, such as establishing a retrieval mode and
goals, initiating and guiding search, and monitoring and verifying
the memories that have been retrieved (for reviews, see Cabeza &
St Jacques, 2007; Gilboa, 2004).
Our findings confirm the constant left-sided recruitment of the
prefrontal cortex in AM retrieval, even concerning its episodic
subcomponent, which contrasts with the right-sided involvement
in episodic memory highlighted by laboratory paradigms. Gilboa
(2004) has demonstrated that the activation of the right prefrontal
cortex (BA 9/46/10) is rarely observed in AM studies, as opposed to
episodic memory studies based on laboratory paradigms. Laboratory activation studies of healthy subjects have shown that the right
prefrontal cortex subtends the retrieval of episodic information
(regardless of its verbal or visuospatial nature), whereas the left pre-
frontal cortex subtends the retrieval of semantic information (see
Hemispheric Encoding/Retrieval Asymmetry model, Habib, Nyberg,
& Tulving, 2003; Tulving et al., 1994). Several interpretations have
been proposed for this preferentially left-sided prefrontal cortex
activation observed in AM studies (for a review, see Cabeza & St
Jacques, 2007; Gilboa, 2004), but we adhere to the view that it may
depend on the nature of generative AM retrieval, which relies on
both executive and semantic processes, even when vivid episodic
AMs are triggered (Conway et al., 2002). This is well in agreement
with the results of Nyberg and his collaborators demonstrating that
AM retrieval, semantic memory and working memory overlap in
left prefrontal cortex (Nyberg et al., 2003).
Our results stressed the involvement of different parts of the
left prefrontal cortex which may reflect the intervention of distinct processes (see Badre & Wagner, 2004; Christoff & Gabrieli,
2000; Petrides, 2000). While our activation studies have mainly
established the existence of left dorsolateral prefrontal activation,
our correlational studies of healthy subjects and frontotemporal
dementia patients have pinpointed the critical role of the left orbitomedial prefrontal cortex (BA 11/47) and, to a lesser extent, that
of the left dorsolateral prefrontal cortex (BA 6/45). Our findings
regarding the left dorsolateral cortex are consistent with its secondary involvement in AM reconstruction (Svoboda et al., 2006),
and suggest that this region is mobilized when high demands are
placed on monitoring processes for certain time periods (e.g. the
most remote one). As regards the orbitomedial (or ventromedial)
prefrontal cortex, this is one of the most ubiquitous activation sites
in AM neuroimaging studies. In fact, although both orbital and dorsolateral areas are associated with executive functions (Cabeza &
Nyberg, 2000; Collette & Van der Linden, 2002), the role of the left
orbitofrontal cortex seems to be more crucial in autobiographical
retrieval (Gilboa, 2004; Svoboda et al., 2006). This could be due
to its involvement in behavioural regulation, emotion or inhibition processing and, of particular relevance here, in the generative
retrieval processes activated in the TEMPau task. Our AM task
probably prompts the assessment of internally generated information and a number of self-referential processes (i.e. representation,
monitoring, assessment and integration of material of a personally
relevant nature, Cabeza & St Jacques, 2007; Northoff & Bermpohl,
2004), and these mainly involve this prefrontal region. Moreover,
Brodmann areas 11 and 47 are closely connected to the limbic structures (Wheeler & Stuss, 2003), this connection being crucial to
episodic AM retrieval (i.e. access attempts and recollection). Therefore, we suggest that the major involvement of the left orbitomedial
prefrontal cortex in the TEMPau task reflects the critical role of
self-referential representation in AM strategic retrieval processes.
Nevertheless, supplementary analyses (based on connectivity or correlation methods and on hypometabolism in one case
study) performed in both types of neuroimaging studies indicated a
more bilateral involvement of the prefrontal cortex in episodic AM
retrieval. This right-hemispheric prefrontal cortex involvement fits
in better with the functional role of this region observed in the
episodic memory retrieval task (Desgranges et al., 1998; Tulving
et al., 1994). In particular, the right orbitomedial prefrontal cortex
matches one of the three right prefrontal cortical sites shown to be
involved not only in the establishment and maintenance of episodic
memory in the “retrieval mode” (Lepage, Ghaffar, Nyberg, & Tulving,
2000), but also in the adoption of self-perspective when remembering past episodes (Northoff & Bermpohl, 2004) and in affectladen autobiographical memory (Markowitsch, Vandekerckhove,
Lanfermann, & Russ, 2003). However, an increasing number of activation studies have detected bilateral prefrontal recruitment during
episodic AM (Greenberg et al., 2005), possibly due to the use of
longer retrieval times (approximately 20 s). Based on electrophysiological findings, Conway et al. (2002) suggested that left prefrontal
activation first appears during the retrieval phase and reflects ini-
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
tiation processes, whereas right prefrontal activations arise later,
along with those of the temporal and posterior regions, when a
memory is held in mind, and reflect access to episodic details via
autobiographical knowledge (i.e. personal semantics), as well as
re-experiencing via autonoetic consciousness.
4.3. The permanent role of the medial temporal lobe in the
recollection of episodic autobiographical memories
The close concordance between our neuropsychological and
functional neuroimaging (activation or correlations) data has
highlighted the involvement of the MTL—and more precisely the
hippocampus—in episodic AM across time. Using strict criteria
for controlling the episodic features of AM, and avoiding certain
methodological biases prevalent in neuroimaging studies, our
present results demonstrate that the recollection of episodic memories is dependent upon the hippocampus whatever their age,
unlike that of semanticized memories (i.e. memories of generic
events or memories associated with Know responses). Importantly,
episodic AMs are characterized by spatiotemporal specificity, but
also by autonoetic consciousness, visual imagery and emotion, all
of which are critical features of episodic memory. We therefore
emphasize that hippocampal involvement is not only related to the
specificity of memories, but also to the sense of “mental time travel”
and phenomenological re-experiencing (Tulving, 2002; Wheeler et
al., 1997). Our studies confirm previous findings that have revealed
not only a common memory retrieval network supporting all AM
types, but also unique regions dedicated to either episodic or
semantic AM (Levine et al., 2004; Maguire & Mummery, 1999),
supporting a functional neuroanatomical dissociation between
episodic and semantic autobiographical memory. The critical
role of the hippocampus in autonoetic consciousness may seem
surprising, given that autonoetic re-experiencing is regarded as a
function that is most likely to be subserved by the frontal lobes.
Nonetheless, this involvement is in keeping with several studies
suggesting that MTL structures, notably the hippocampus, do
indeed play a part in this phenomenon (Moscovitch et al., 2005;
Tulving & Markowitsch, 1998).
The involvement of the hippocampus in episodic AM retrieval
whatever the lifetime period argues against the Standard Theory
of consolidation and instead supports the Multiple Trace Theory, which states that the MTL is involved in the mechanism that
reactivates all the neocortical regions where the multifaceted components of episodic memories are represented, regardless of the
passage of time (see Section 1). Further strong arguments are
additionally provided, as we underline the permanent nature of
the connectivity between the MTL and neocortex (more specifically the temporal region) in healthy subjects, both for remote and
recent episodic AMs, as predicted by the Multiple Trace Theory
(Moscovitch et al., 2005; Nadel, Winocur, Ryan, & Moscovitch, 2007;
Nadel, Campbell, et al., 2007). However, our results also show, and
confirm, that memory remoteness is not the only factor influencing
brain MTL activity, as the phenomenological features of episodic
AM retrieval are also crucial for the continuous involvement of
MTL-neocortical connectivity over time (see also Moscovitch et
al., 2005). For example, we found that remote or recent periods
which were richer in phenomenal qualities prompted bilateral hippocampal activation, whereas remote or recent periods which were
episodic in terms of specificity and details but with a lower level
of re-experiencing and phenomenological features gave rise to
left hippocampal activation instead. Further arguments are provided, showing that the various phenomenological attributes of
episodic AMs, such as re-experiencing and mental visual imagery
(i.e., retrieval strategy used, number of images, field point of
view), are predictive of hippocampal involvement (both in activation and correlation studies), chiefly right-sided. Like Piefke et al.
13
(2003), we found that positive emotional attributes predicted bilateral hippocampal activation. In the same vein, we also observed
that within-MTL connectivity (hippocampus, parahippocampus
and amygdala) and MTL-neocortical connectivity was greater for
richly recollected episodic AMs, regardless of their remoteness, in
line with the recent study of Nadel, Campbell, et al. (2007) which
showed that hippocampal–neocortical activation is not influenced
by the passage of time (but by multiple retrievals of AM). Lastly,
we demonstrated that recollected factual, spatial and temporal
elements of specific AMs (Remember responses justified by the
recollection of contextual details) were connected to right-sided
hippocampal activity. As far as the correlation studies are concerned, the pivotal role of the right hippocampus can be explained
by the fact that we used a special episodic AM task designed to
prompt the re-experiencing associated with AM retrieval, as well as
by the other AM qualities accompanying this re-experiencing. Our
overall results suggest that the bilateral or right hippocampus contributes to the successful retrieval of episodic memories, which is
largely dependent upon the richness of the phenomenological and
spatiotemporal details that are re-experienced, above and beyond
their specificity. Recollection was therefore found to be an important determinant of hippocampal activation in terms of the ability
to re-experience events and the other AM qualities associated with
re-experiencing, such as detail, emotionality, visual imagery and
personal significance, all these features being described as important characteristics of episodic AMs, contributing to autonoetic
consciousness.
Finally, the issue of hippocampal laterality in AM remains the
subject of much debate. In keeping with our lesion study in epileptic patients, Gilboa et al. (2005), unlike Kopelman et al. (2003),
found a significant correlation in patients with AD between remote
AM and the amount of remaining tissue in bilateral MTL. This
correlation was stronger on the right than on the left, while personal semantic memory was mainly related to a pattern of bilateral
anterior and posterior lateral temporal cortex decline, which was
more pronounced on the left. We also reported a link between
right MTL glucose metabolism in AD patients and recent episodic
AMs (unlike semanticized remote AMs). Regarding our activation studies, the results differ from most neuroimaging studies of
AM, which have reported the constant involvement of the hippocampus, preferentially left-lateralized like the prefrontal cortex
(Maguire, 2001). Some studies have suggested that a more bilateral network may be activated in frontal and medial temporal
regions during episodic AM retrieval, depending on the recency
of memories (Maguire & Frith, 2003b), as well as the age of the
subjects (for a review, see Piefke & Fink, 2005) and the presence
of amnesia (Maguire, Vargha-Khadem, & Mishkin, 2001). A reduction in hemispheric asymmetry (see the Hemispheric Asymmetry
Reduction in OLDder adults model of ageing effects, Cabeza, 2002)
could account for the bilateral involvement of the hippocampus,
suggesting in turn the existence of compensatory processes. However, our results are in keeping with recent data revealing that
the re-experiencing of recollected memories and the qualities of
these memories may influence hippocampal engagement independently of factors such as remoteness and age. For example, some
activation studies have detected bilateral or right hippocampal activation when subjects, regardless of their age, become engaged in
the retrieval of specific autobiographical memories rated highly in
terms of mental imagery, richness of detail, emotionality, reexperiencing or personal significance (Addis, Moscovitch, Crawley, &
McAndrews, 2004; Daselaar et al., 2008; Greenberg et al., 2005;
Markowitsch et al., 2000; Piefke et al., 2003; Steinvorth, Corkin, &
Halgren, 2006). Overall findings suggest that, above and beyond
the specificity of memories which may be sustained by the left
hippocampus, the phenomenological qualities of memories may
activate the bilateral or right hippocampus.
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
14
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
In summary, the findings of our activation and correlation
studies of healthy subjects and our neuropsychological and neuroimaging studies of epileptic patients stress the role of the bilateral
or right MTL in the recollection of rich recent and remote episodic
AMs. Interestingly, however, they indicate that the Multiple Trace
Theory (and more generally models of memory consolidation)
could be supplemented and possibly strengthened by a more
accurate consideration of the way in which the MTL-neocortical
interaction is modulated by the phenomenal features of memories that are retrieved, such as re-experiencing, emotion and self
perspective, or frequency of AM retrievals (see Nadel, Winocur, et
al., 2007; Nadel, Campbell, et al., 2007). As stressed recently by
Moscovitch (2008), the exact role of hippocampus regarding the
complex reconstructive processes in episodic memory over the
course of time is one of the key challenges of current cognitive
neuroscience.
In conclusion, as Tulving (2002) explains, “people can have
mental access to their personal past not only in terms of autonoetic remembering but also in terms of nonautonoetic knowing”
(p. 7). By developing a paradigm specifically designed to assess
the three prerequisites of episodic autobiographical memories –
self, autonoetic consciousness and subjectively sensed time – we
have shown that knowing develops before remembering in children and that remembering is more susceptible to deterioration
over time and with age, as well as in most patients with cerebral
lesions, with different profiles corresponding to different situations.
Our present data, based on neuropsychological and neuroimaging studies, highlight the importance of the phenomenological self
in maintaining a sense of continuity in subjective time, and of
the prefrontal lobe in implementing self-related retrieval strategies and hippocampus in re-experiencing the past regardless of its
remoteness. At the cognitive and neural level, they also reveal the
complexity of the constructive and dynamic nature of episodic AMs
over time.
The study of episodic AMs confirms that episodic memory is
“really a marvel of nature” (Tulving, 2002, p. 19), and the richness of these episodic AMs will undoubtedly prove particularly
useful for honing the concept of episodic memory still further.
As Endel Tulving has written, “It took biological evolution a long
time to build a time machine in the brain, and it has managed
to do it only once, but the consequences have been enormous:
by virtue of their mental control over time, human beings now
wield powers on Earth that in many ways rival or even exceed
those of nature itself. It is difficult to imagine a marvel of nature
greater than that.” (Tulving, 2002, p. 20). Another vital task will
be to continue making the study of AM (and its two components, i.e. episodic memory and semantic memory) a more integral
part of models of human memory (Eustache & Desgranges, 2008;
Piolino, Desgranges, & Eustache, 2008). Last but not least, it will
be particularly rewarding to continue our cognitive and neural
exploration of the interactions between autobiographical memory and working memory (Baddeley, 2000), perceptual memory
(Gagnepain, Lebreton, Desgranges, & Eustache, 2008), and procedural memory (Beaunieux et al., 2006). A truly exciting prospect
indeed!
Acknowledgements
An earlier version of this paper was presented at a meeting held
in honour of Professor Tulving (Tallinn, 2007). The authors would
particularly like to thank E. Tulving for being such an inexhaustible
source of inspiration for our research on memory. They also thank G.
Chételat, C. Duval, G. Giffard-Quillon, K. Lebreton, V. Matuszewski,
M. Noulhiane, L. Picard and A. Viard for their valuable contribution
to the studies described in this paper, and E. Portier-Wiles for her
help in the English style.
References
Addis, R. A., & Tippet, L. J. (2004). Memory of myself: Autobiographical memory and
identity in Alzheimer’s disease. Memory, 12, 56–74.
Addis, D. R., Moscovitch, M., Crawley, A. P., & McAndrews, M. P. (2004). Recollective
qualities modulate hippocampal activation during autobiographical memory
retrieval. Hippocampus, 14, 752–762.
Baddeley, A. D. (2000). The episodic buffer: A new component of working memory.
Trends in Cognitive Sciences, 4(11), 417–423.
Baddeley, A. D. (2001). The concept of episodic memory. Philosophical Transactions
of the Royal Society of London, Series B, Biological Sciences, 356, 1545–1550.
Badre, D., & Wagner, A. D. (2004). Selection, integration, and conflict monitoring:
Assessing the nature and generality of prefrontal cognitive control mechanisms.
Neuron, 41, 473–487.
Bayley, P. J., Gold, J. J., Hopkins, R. O., & Squire, L. R. (2005). The neuroanatomy of
remote memory. Neuron, 2, 799–810.
Beaunieux, H., Hubert, V., Witkowski, T., Pitel, A. L., Rossi, S., Danion, J. M., et al. (2006).
Which processes are involved in cognitive procedural learning? Memory, 14(5),
521–539.
Bernard, F. A., Bullmore, E. T., Graham, K. S., Thompson, S. A., Hodges, J. R., & Fletcher,
P. C. (2004). The hippocampal region is involved in successful recognition of both
remote and recent famous faces. Neuroimage, 22(4), 1704–1714.
Bluck, S. (2003). Autobiographical memory: Exploring its functions in everyday life.
Memory, 11, 113–123.
Borrini, G., Dall’Ora, P., Della Sala, S., Marinelli, L., & Spinnler, H. (1989). Autobiographical memory, sensitivity to age and education of a standardized inquiry.
Psychological Medicine, 19, 215–224.
Brewer, W. (1996). What is recollective memory? In D. C. Rubin (Ed.), Remembering
our past: Studies in autobiographical memory (pp. 19–66). Cambridge, England:
Cambridge University Press.
Bright, P., Buckman, J., Fradera, A., Yoshimasu, H., Colchester, A. C., & Kopelman, M.
D. (2006). Retrograde amnesia in patients with hippocampal, medial temporal,
temporal lobe, or frontal pathology. Learning and Memory, 13, 545–557.
Burianova, H., & Grady, C. L. (2007). Common and unique neural activations in autobiographical, episodic, and semantic retrieval. Journal of Cognitive Neuroscience,
19, 1520–1534.
Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: the HAROLD
model. Psychology and Aging, 17(1), 85–100.
Cabeza, R., & Nyberg, L. (2000). Imaging cognition II: An empirical review of 275 PET
and fMRI studies. Journal of Cognitive Neuroscience, 12, 1–47.
Cabeza, R., & St Jacques, P. (2007). Functional neuroimaging of autobiographical
memory. Trends in Cognitive Sciences, 11, 219–227.
Cermak, L. S. (1984). The episodic-semantic distinction in amnesia. In L. R. Squire
& N. Butters (Eds.), Neuropsychology of memory (pp. 55–62). New York: Guilford
Press.
Chateaubriand, R. F. (1848). Mémoires d’outre-tombe, tome 1: Livres I à XII, Livre de
Poche.
Christoff, K., & Gabrieli, J. D. E. (2000). The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human
prefrontal cortex. Psychobiology, 28, 168–186.
Clarys, D., Isingrini, M., & Gana, K. (2002). Mediators of age related differences in
recollective experience. Acta Neurologica Belgica, 109, 315–329.
Coles, J. P., Fryer, T. D., Bradley, P. G., Nortje, J., Smielewski, P., Rice, K., et al. (2006).
Intersubject variability and reproducibility of 15O PET studies. Journal of Cerebral
Blood Flow and Metabolism, 26, 48–57.
Collette, F., & Van der Linden, M. (2002). Brain imaging of the central executive
component of working memory. Neuroscience and Biobehavioural Review, 26,
105–125.
Conway, M. A., & Fthenaki, A. (2000). Disruption and loss of autobiographical memory. In L. S. Cermak (Ed.), Handbook of neuropsychology: Memory and its disorders
(pp. 257–288). Amsterdam: Elsevier.
Conway, M. A., & Pleydell-Pearce, C. W. (2000). The construction of autobiographical memories in the self-memory system. Psychological Review, 107, 261–
288.
Conway, M. A., Gardiner, J. M., Perfect, T. J., Anderson, S. J., & Cohen, G. M. (1997).
Changes in memory awareness during learning: The acquisition of knowledge
by psychology undergraduates. Journal of Experimental Psychology: General, 126,
393–413.
Conway, M. A., Pleydell-Pearce, C. W., Whitecross, S. E., & Sharpe, H. (2002). Brain
imaging autobiographical memory. The Psychology of Learning and Motivation:
Advances in Research and Theory, 41, 229–263.
Conway, M. A., Singer, J. A., & Tagini, A. (2004). The self and autobiographical memory:
Correspondence and coherence. Social Cognition, 22, 491–529.
Crawley, S. E., & French, C. C. (2005). Field and observer viewpoint in remember/know
memories of personal childhood events. Memory, 13, 673–681.
Crovitz, H. F., & Schiffman, H. (1974). Frequency of episodic memories as a function
of their age. Bulletin of the Psychonomic Society, 4, 517–551.
Damasio, A. R. (1989). Time-locked multiregional retroactivation: A systems-level
proposal for the neural substrates of recall and recognition. Cognition, 33(1–2),
25–62.
Danion, J. M., Cuervo, C., Piolino, P., Huron, C., Riutort, M., Peretti, C. S., et al. (2005).
Abnormal subjective sense of self in patients with schizophrenia. Consciousness
and Cognition, 14, 535–547.
Daselaar, S. M., Rice, H. J., Greenberg, D. L., Cabeza, R., Labar, K. S., & Rubin, D. C. (2008).
The spatiotemporal dynamics of autobiographical memory: Neural correlates of
recall, emotional intensity, and reliving. Cerebral Cortex, 18, 217–229.
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
Desgranges, B., Baron, J. C., de la Sayette, V., Petit-Taboué, M. C., Benali, K., Landeau, B., et al. (1998). The neural substrates of memory systems impairment
in Alzheimer’s disease. A PET study of resting brain glucose utilization. Brain,
121, 611–631.
Desgranges, B., Baron, J. C., Laleveé, C., Giffard, B., Viader, F., de la Sayette, V., et al.
(2002). The neural substrates of episodic memory impairment in Alzheimer’s
disease as revealed by FDG-PET: Relationship to degree of deterioration. Brain,
125, 1116–1124.
Duval, C., Eustache, F., & Piolino, P. (2007). Multidimensional self, autobiographical memory and aging. Psychologie et Neuropsychiatrie du Vieillissement, 5, 178–
192.
Eustache, F., & Desgranges, B. (2008). MNESIS: Towards the integration of current
multisystem models of memory. Neuropsychological Review, 18(1), 53–69.
Eustache, F., Desgranges, B., Giffard, B., de la Sayette, V., & Baron, J. C. (2001). Entorhinal cortex disruption causes memory deficit in early Alzheimer’s disease as
shown by PET. Neuroreport, 12, 683–685.
Eustache, F., Piolino, P., Giffard, B., Viader, F., de la Sayette, V., Baron, J. C., et al. (2004).
‘In the course of time’: A PET study of the cerebral substrates of autobiographical
amnesia in Alzheimer’s disease. Brain, 127, 1549–1560.
Fitzgerald, J. M. (1996). Vivid memories and the reminiscence phenomenon: The role
of a self narrative. Human Development, 31, 261–270.
Freud, S. (1905). Trois essais sur la théorie de la sexualité. Paris: Payot.
Gagnepain, P., Lebreton, K., Desgranges, B., & Eustache, F. (2008). Perceptual priming
enhances the creation of new episodic memories. Consciousness and Cognition,
17(1), 276–287.
Gardiner, J. M. (1988). Functional aspects of recollective experience. Memory and
Cognition, 16, 309–313.
Gardiner, J. M. (2001). Episodic memory and autonoetic consciousness: A firstperson approach. Philosophical Transactions of the Royal Society, 356, 1351–
1361.
Gardiner, J. M., Ramponi, C., & Richardson-Klavehn, A. (1998). Experiences of remembering, knowing, and guessing. Consciousness and Cognition, 7, 1–26.
Gilboa, A. (2004). Autobiographical and episodic memory-one and the same? Evidence from prefrontal activation in neuroimaging studies. Neuropsychologia, 42,
1336–1349.
Gilboa, A., Winocur, G., Grady, C. L., Hevenor, S. J., & Moscovitch, M. (2004). Remembering our past: Functional neuroanatomy of recollection of recent and very
remote personal events. Cerebral Cortex, 14, 1214–1225.
Gilboa, A., Ramirez, J., Köhler, S., Westmacott, R., Black, S. E., & Moscovitch, M.
(2005). Retrieval of autobiographical memory in Alzheimer’s disease: Relation
to volumes of medial temporal lobe and other structures. Hippocampus, 15(4),
535–550.
Greenberg, D. L., & Rubin, D. C. (2003). The neuropsychology of autobiographical
memory. Cortex, 39, 687–728.
Greenberg, D. L., Rice, H. J., Cooper, J. J., Cabeza, R., Rubin, D. C., & Labar, K. S. (2005).
Co-activation of the amygdala, hippocampus and inferior frontal gyrus during
autobiographical memory retrieval. Neuropsychologia, 43, 659–674.
Guillery, B., Desgranges, B., Piolino, P., Laville, P., de la Sayette, V., & Eustache, F.
(2000). Extensive temporally graded retrograde amnesia for personal-episodic
facts in transient global amnesia. Neurocase, 6, 205–210.
Habib, R., Nyberg, L., & Tulving, E. (2003). Hemispheric asymmetries of memory: the
HERA model revisited. Trends in Cognitive Sciences, 7(6), 241–245.
Ivaniou, A., Cooper, J. M., Shanks, M. F., & Venneri, A. (2006). Patterns of impairment
in autobiographical memory in the degenerative dementias constrain models of
memory. Neuropsychologia, 44, 1936–1955.
James, W. (1890). Principles of psychology. Chicago: University of Chicago Press.
Johnson, M. K., Foley, M. A., Suengas, A. G., & Raye, C. L. (1988). Phenomenal characteristics of memories for perceived and imagined autobiographical events. Journal
of Experimental Psychology: General, 117(4), 371–376.
Kopelman, M. D. (2000). The neuropsychology of remote memory. In L. Cermak (Ed.),
Handbook of neuropsychology (pp. 251–280). Amsterdam: Elsevier.
Kopelman, M. D., & Kapur, N. (2001). The loss of episodic memories in retrograde
amnesia: Single-case and group studies. Philosophical Transactions of the Royal
Society of London. Series B, Biological sciences, 356, 1409–1421.
Kopelman, M. D., Wilson, B. A., & Baddeley, A. D. (1989). The autobiographical memory interview: A new assessment of autobiographical and personal semantic
memory in amnesic patients. Journal of Clinical and Experimental Neuropsychology, 11, 724–744.
Kopelman, M. D., Lasserson, D., Kingsley, D. R., Bello, F., Rush, C., Stanhope, N., et
al. (2003). Retrograde amnesia and the volume of critical brain structures. Hippocampus, 13(8), 879–891.
Lemogne, C., Piolino, P., Friszer, S., Claret, A., Girault, N., Jouvent, R., et al. (2006).
Episodic autobiographical memory in depression: Specificity, autonoetic consciousness and self-perspective. Consciousness and Cognition, 15, 258–268.
Lemogne, C., Bergouignan, L., Piolino, P., Jouvent, R., Allilaire, J. F., & Fossati, P.
(2009). Cognitive avoidance of intrusive memories and autobiographical memory: Specificity, autonoetic consciousness, and self-perspective. Memory, 17(1),
1–7.
Lepage, M., Habib, R., & Tulving, E. (1998). Hippocampal PET activations of memory
encoding and retrieval: The HIPER model. Hippocampus, 8, 313–322.
Lepage, M., Ghaffar, O., Nyberg, L., & Tulving, E. (2000). Prefrontal cortex and episodic
memory retrieval mode. The Proceedings of the National Academy of Sciences (US),
97, 506–511.
Levine, B., Black, S. E., Cabeza, R., Sinden, S., Meintosh, A. R., Toth, J. P., et al. (1998).
Episodic memory and the self in a case of isolated retrograde amnesia. Brain,
121, 1951–1973.
15
Levine, B., Svoboda, E., Hay, J. F., Winocur, G., & Moscovitch, M. (2002). Aging and autobiographical memory: Dissociating episodic from semantic memory. Psychology
and Aging, 17, 677–689.
Levine, B., Turner, G. R., Tisserand, D., Hevenor, S. J., Graham, S. J., & McIntosh,
A. R. (2004). The functional neuroanatomy of episodic and semantic autobiographical remembering: A prospective functional MRI study. Journal of Cognitive
Neuroscience, 16, 1633–1646.
Libby, L. K., & Eibach, R. P. (2002). Looking back in time: Self-concept change affects
visual perspective inautobiographical memory. Journal of Personality and Social
Psychology, 82, 167–179.
Linton, M. (1986). Ways of searching and the contents of memory. In D. C. Rubin
(Ed.), Autobiographical memory (pp. 50–67). Cambridge, England: Cambridge
University Press.
Locke, J. (1690/1975). An essay concerning human understanding. Oxford: Oxford University Press.
Maguire, E. A. (2001). Neuroimaging studies of autobiographical event memory.
Philosophical transactions of the Royal Society of London. Series B. Biological Sciences, 356, 1441–1451.
Maguire, E. A., & Frith, C. D. (2003a). Aging affects the engagement of the hippocampus during autobiographical memory retrieval. Brain, 126, 1511–1523.
Maguire, E. A., & Frith, C. D. (2003b). Lateral asymmetry in the hippocampal response
to the remoteness of autobiographical memories. Journal of Neuroscience, 23,
5302–5307.
Maguire, E. A., & Mummery, C. J. (1999). Differential modulation of a common memory retrieval network revealed by positron emission tomography. Hippocampus,
9, 54–61.
Maguire, E. A., Vargha-Khadem, F., & Mishkin, M. (2001). The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory
retrieval. Brain, 124, 1156–1170.
Markowitsch, H. J. (1995). Which brain regions are critically involved in the retrieval
of old episodic memory? Brain Research Review, 21, 117–127.
Markowitsch, H. J., Thiel, A., Reinkemeier, M., Kessler, J., Koyuncun, A., & Heiss, W. D.
(2000). Right amygdalar and temporofrontal activation during autobiographic,
but not fictitious memory retrieval. Behavioral Neurology, 12, 181–190.
Markowitsch, H. J., Vandekerckhove, M. M., Lanfermann, H., & Russ, M. O. (2003).
Engagement of lateral and medial prefrontal areas in the ecphory of sad and
happy autobiographical memories. Cortex, 39, 643–665.
Matuszewski, V., Piolino, P., de la Sayette, V., Lalevée, C., Pèlerin, A., Dupuy, B., et al.
(2006). Retrieval mechanisms for autobiographical memories: Insights from the
frontal variant of frontotemporal dementia. Neuropsychologia, 44, 2386–2397.
Matuszewski, V., Piolino, P., Belliard, S., Lalevée, C., Pèlerin, A., De la Sayette, V., et al.
(in press). Mechanisms of disruption of autobiographical memories in semantic
dementia. Cortex.
Mc Gaugh, J. L. (2000). Memory—A century of consolidation. Science, 287, 248–251.
Meeter, M., & Murre, J. M. (2004). Consolidation of long-term memory: Evidence and
alternatives. Psychological Bulletin, 130, 843–857.
Moscovitch, M. (2008). The hippocampus as a “Stupid,” domain-specific module:
Implications for theories of recent and remote memory, and of imagination.
Canadian Journal of Experimental Psychology, 62(1), 62–79.
Moscovitch, M., Yaschyshyn, T., Ziegler, M., & Nadel, L. (1999). Remote episodic memory and retrograde amnesia: Was Endel Tulving right all along? In E. Tulving
(Ed.), Memory, consciousness, and the brain: The Tallinn conference (pp. 331–345).
Philadelphia, PA: Psychology Press.
Moscovitch, M., Rosenbaum, R. S., Gilboa, A., Addis, D. R., Westmacott, R., Grady, C.,
et al. (2005). Functional neuroanatomy of remote episodic, semantic and spatial
memory: A unified account based on multiple trace theory. Journal of Anatomy,
207, 35–66.
Moss, E., Cappelletti, M., De Mornay Davies, P., Jaldow, E., & Kopelman, M. (2000). Lost
for words or loss of memories: Autobiographical memory in semantic dementia.
Brain and Language, 74, 350–354.
Nadel, L., & Moscovitch, M. (1997). Memory consolidation, retrograde amnesia and
the hippocampal complex. Current Opinion in Neurobiology, 7, 217–227.
Nadel, L., Winocur, G., Ryan, L., & Moscovitch, M. (2007). Systems consolidation and
hippocampus: Two views. Debates in Neuroscience, 1, 55–66.
Nadel, L., Campbell, J., & Ryan, L. (2007). Autobiographical memory retrieval and
hippocampal activation as a function of repetition and the passage of time. Neural
Plasticity, 90472.
Nelson, K., & Fivush, R. (2004). The emergence of autobiographical memory: A social
cultural developmental theory. Psychological Review, 111, 486–511.
Nestor, P. J., Graham, K. S., Bozeat, S., Simons, J. S., & Hodges, J. R. (2002). Memory
consolidation and the hippocampus: Further evidence from studies of autobiographical memory in semantic dementia and frontal variant of frontotemporal
dementia. Neuropsychologia, 40, 633–654.
Nigro, G., & Neisser, U. (1983). Point of view in personal memories. Cognitive Psychology, 15, 467–482.
Niki, K., & Luo, J. (2002). An fMRI study on the time-limited role of the medial temporal lobe in long-term topographical autobiographic memory. Journal of Cognitive
Neuroscience, 14, 500–507.
Noël, A., Quinette, P., Guillery-Girard, B., Dayan, J., Piolino, P., Marquis, S., et al. (2008).
Psychopathological factors, memory disorders and transient global amnesia.
British Journal of Psychiatry, 193(2), 145–151.
Northoff, G., & Bermpohl, F. (2004). Cortical midline structures and the Self. Trends
in Cognitive Sciences, 8, 102–107.
Noulhiane, M., Piolino, P., Hasboun, D., Baulac, M., & Samson, S. (2007). Autobiographical memory after temporal lobe resection: Neuropsychological and MRI
volumetric findings. Brain, 130, 3184–3199.
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020
G Model
NSY-3193; No. of Pages 16
16
ARTICLE IN PRESS
P. Piolino et al. / Neuropsychologia xxx (2009) xxx–xxx
Noulhiane, M., Piolino, P., Hasboun, D., Baulac, M., & Samson, S. (2008). Autobiographical memory and autonoetic consciousness following temporal lobe resection.
Journal of Behavioral Neurology, 19(1–2), 19–22.
Nyberg, L., Forkstam, C., Petersson, M., Cabeza, R., & Ingvar, M. (2002). Brain imaging
of human memory systems: between-systems similarities and within-system
differences. Cognitive Brain Research, 13, 281–292.
Nyberg, L., Marklund, L., Persson, J., Cabeza, R., Forkstam, C., Petersson, K. M., et
al. (2003). Common prefrontal activations during working memory, episodic
memory, and semantic memory. Neuropsychologia, 41, 371–377.
Okuda, J., Fujii, T., Ohtake, H., Tsukiura, T., Tanji, K., Suzuki, K., et al. (2003). Thinking
of the future and past: The roles of the frontal pole and the medial temporal
lobes. Neuroimage, 19, 1369–1380.
Perfect, T. J., & Dasgupta, Z. R. (1997). What underlies the deficit in reported recollective experience in old age? Memory and Cognition, 25, 849–858.
Parkin, A. J., & Walter, B. M. (1992). Recollective experience, normal aging, and frontal
dysfunction. Psychology and Aging, 7, 290–298.
Petrides, M. (2000). Frontal lobe and memory. In F. Boller & J. Grafman (Eds.), Handbook of neuropsychology (2nd ed., 2, pp. 67–84). Amsterdam: Elsevier.
Piefke, M., & Fink, G. R. (2005). Recollections of one’s own past: the effects of aging
and gender on the neural mechanisms of episodic autobiographical memory.
Anatomy and Embryology, 210(5–6), 497–512.
Piefke, M., Weiss, P. H., Zilles, K., Markowitsch, H. J., & Fink, G. R. (2003). Differential
remoteness and emotional tone modulate the neural correlates of autobiographical memory. Brain, 126, 650–668.
Piolino, P. (2008). Evaluation et prise en charge des troubles de la mémoire autobioghique en neuropsychologie. In P. Piolino, C. Thomas-Antérion, & F. Eustache
(Eds.), Des amnésies organiques aux amnésies psychogènes: théorie, pratique et prise
en charge. Marseille: Solal, pp. 339–388.
Piolino, P., Desgranges, B., & Eustache, B. (2000). La mémoire autobiographique:
Théorie et pratique [Autobiographical memory: Theory and practice]. Marseille,
France: Solal.
Piolino, P., Desgranges, B., Benali, K., & Eustache, F. (2002). Episodic and semantic
remote autobiographical memory in ageing. Memory, 10, 239–257.
Piolino, P., Desgranges, B., Belliard, S., Matuszewski, V., Lalevée, C., De la Sayette, V.,
et al. (2003). Autobiographical memory and autonoetic consciousness: Triple
dissociation in neurodegenerative diseases. Brain, 126, 2203–2219.
Piolino, P., Belliard, S., Desgranges, B., Perron, M., & Eustache, F. (2003). Autobiographical memory and autonoetic consciousness in a case of semantic dementia.
Cognitive Neuropsychology, 20, 619–639.
Piolino, P., Giffard-Quillon, G., Desgranges, B., Chételat, G., Baron, J. C., & Eustache, F.
(2004). Re-experiencing old memories via hippocampus: A PET study of autobiographical memory. Neuroimage, 22, 1371–1383.
Piolino, P., Hannequin, D., Desgranges, B., Girard, B., Beaunieux, H., Giffard, B., et
al. (2005). Right ventral frontal hypometabolism and abnormal sense of self in
a case of disproportionate retrograde amnesia. Cognitive Neuropsychology, 22,
1005–1034.
Piolino, P., Desgranges, B., Clarys, D., Guillery-Girard, B., Taconnat, L., Isingrini, M.,
et al. (2006). Autobiographical memory, autonoetic consciousness and selfperspective in aging. Psychology and Aging, 21, 510–525.
Piolino, P., Lamidey, V., Desgranges, B., & Eustache, F. (2007). The semantic and
episodic subcomponents of famous person knowledge: Dissociation in healthy
subjects. Neuropsychology, 21, 122–135.
Piolino, P., Hisland, M., Matuszewski, V., Jambaqué, I., & Eustache, F. (2007). Do
school-age children remember or know the personal past? Consciousness and
Cognition, 16, 84–101.
Piolino, P., Chételat, G., Matuszewski, V., Landeau, B., Mézenge, F., Viader, F., et al.
(2007). In search of autobiographical memories: A PET study in the frontal variant of frontotemporal dementia. Neuropsychologia, 45, 2730–2743.
Piolino, P., Desgranges, B., Manning, L., North, P., Jokic, F., & Eustache, F. (2007). Autobiographical memory, the sense of recollection and executive functions after
severe closed head injury. Cortex, 43, 176–195.
Piolino, P., Desgranges, B., Hubert, V., Bernard, F., Chételat, G., Baron, J. C., et al. (2008).
Reliving lifelong episodic autobiographical memories via the hippocampus: A
correlative resting PET study in healthy middle-aged subjects. Hippocampus, 18,
445–459.
Piolino, P., Desgranges, B., & Eustache, F. (2008). A la recherche du self: modèles
et bases neurales de la mémoire autobiographique. In P. Piolino, C. ThomasAntérion, & F. Eustache (Eds.), Des amnésies organiques aux amnésies psychogènes:
théorie, pratique et prise en charge. Marseille: Solal, pp. 89–126.
Rauchs, G., Piolino, P., Mézenge, F., Landeau, B., Lalevée, C., Pèlerin, A., et al. (2007).
Autonoetic consciousness in Alzheimer’s disease: Neuropsychological and PET
findings using an episodic learning and recognition task. Neurobiology of Aging,
28, 1410–1420.
Ribot, T. (1881). Les maladies de la mémoire. Paris: Germer-Bailliere.
Robinson, J. A., & Swanson, S. (1993). Autobiographical memory: The next phase.
Applied Cognitive Psychology, 4, 321–335.
Rosenbaum, R. S., Köhler, S., Schacter, D. L., Moscovitch, M., Westmacott, R., Black, S.
E., et al. (2005). The case of K.C.: Contributions of a memory-impaired person to
memory theory. Neuropsychologia, 43(7), 989–1021.
Rubin, D. C., & Berntsen, D. (2003). Life scripts help to maintain autobiographical memories of highly positive, but not highly negative, events. Memory and
Cognition, 31(1), 1–14.
Rubin, D. C., & Kozin, M. (1984). Vivid memories. Cognition, 16(1), 81–95.
Rubin, D. C., & Schulkind, M. D. (1997). The distribution of autobiographical memories
across the life span. Memory and Cognition, 25, 859–866.
Rubin, D. C., Wetzler, S. E., & Nebes, R. D. (1986). Autobiographical memory across the
lifespan. In D. C. Rubin (Ed.), Autobiographical memory (pp. 202–221). Cambridge,
England: Cambridge University Press.
Rubin, D. C., Rahhal, T. A., & Poon, L. W. (1998). Things learned in early adulthood are
remembered best. Memory and Cognition, 26, 3–19.
Rybash, J. M., & Monaghan, B. E. (1999). Episodic and semantic contributions to older
adults’ autobiographical recall. Journal of General Psychology, 126, 85–96.
Salmon, E., Lekeu, F., Bastin, C., Garraux, G., & Collette, F. (2008). Functional imaging of cognition in Alzheimer’s disease using positron emission tomography.
Neuropsychologia, 46(6), 1613–1623.
Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal
lesions. Journal of Neurology Neurosurgery and Psychiatry, 20, 11–21.
Squire, L. R., & Alvarez, P. (1995). Retrograde amnesia and memory consolidation: A
neurobiological perspective. Current Opinion in Neurobiology, 5, 169–177.
Steinvorth, S., Corkin, S., & Halgren, E. (2006). Ecphory of autobiographical memories:
An fMRI study of recent and remote memory retrieval. Neuroimage, 30, 285–298.
Svoboda, E., McKinnon, M. C., & Levine, B. (2006). The functional neuroanatomy of
autobiographical memory: A meta-analysis. Neuropsychologia, 44, 2189–2208.
Talarico, J. M., Labar, K. S., & Rubin, D. C. (2004). Emotional intensity predicts autobiographical memory experience. Memory and Cognition, 32, 1118–1132.
Teipel, S. J., Willoch, F., Ishii, K., Bürger, K., Drzezga, A., Engel, R., et al. (2006). Resting state glucose utilization and the CERAD cognitive battery in patients with
Alzheimer’s disease. Neurobiology and Aging, 27, 681–690.
Tulving, E. (1985). Memory and consciousness. Canadian Psychologist, 25, 1–12.
Tulving, E. (1993). Self-knowledge of an amnesic individual is represented abstractly.
In T. K. Srull & R. S. Wyer (Eds.), Mental representation of trait and autobiographical
knowledge about the self (pp. 147–157). Hillsdale, NJ: Erlbaum.
Tulving, E. (2001). Episodic and common sense: How far apart? Philosophical Transactions of the Royal Society of London, 356, 1505–1515.
Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53, 1–25.
Tulving, E., & Markowitsch, H. J. (1998). Episodic and declarative memory: Role of
the hippocampus. Hippocampus, 8, 198–204.
Tulving, E., Schacter, D. L., McLachlan, D. R., & Moscovitch, M. (1988). Priming of
semantic autobiographical knowledge: A case study of retrograde amnesia. Brain
and Cognition, 8, 3–20.
Tulving, E., Kapur, S., Craik, F. I. M., Moscovitch, M., & Houle, S. (1994). Hemispheric
encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. The Proceedings of the National Academy of Sciences (US), 91,
2016–2020.
Tulving, E., Habib, R., Nyberg, L., Lepage, M., & McIntosh, A. R. (1999). Positron
emission tomography correlations in and beyond medial temporal lobes. Hippocampus, 9, 71–82.
Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connelly, A., Van Paesschen, W.,
& Mishkin, M. (1997). Differential effects of early hippocampal pathology on
episodic and semantic memory. Science, 277, 5324–5376.
Viard, A., Piolino, P., Desgranges, B., Chételat, G., Lebreton, K., Landeau, B., et al. (2007).
Hippocampal activation for autobiographical memories over the entire lifetime
in healthy aged subjects: An fMRI study. Cerebral Cortex, 17, 2453–2467.
Viard, A., Lebreton, K., Chételat, G., Desgranges, B., Landeau, B., Young, A., et al. (submitted). Patterns of hippocampal–neocortical connectivity in the retrieval of
episodic autobiographical memories across the entire life-span of aged adults.
Viskontas, I. V., McAndrews, M. P., & Moscovitch, M. (2000). Remote episodic memory
deficits in patients with unilateral temporal lobe epilepsy and excisions. Journal
of Neuroscience, 20, 5853–5857.
Westmacott, R., & Moscovitch, M. (2003). The contribution of autobiographical significance to semantic memory. Memory and Cognition, 31, 761–774.
Westmacott, R., Leach, L., Freedman, M., & Moscovitch, M. (2001). Different patterns of autobiographical memory loss in semantic dementia and medial
temporal lobe amnesia: A challenge to consolidation theory. Neurocase, 7,
37–55.
Wheeler, M. A., & McMillan, C. T. (2001). Focal retrograde amnesia and the episodicsemantic distinction. Cognitive and Affective Behavioral Neurosciences, 1, 22–36.
Wheeler, M. A., & Stuss, D. T. (2003). Remembering and knowing in patients with
frontal lobe injuries. Cortex, 39, 827–846.
Wheeler, M. A., Stuss, D. T., & Tulving, E. (1997). Toward a theory of episodic memory: The frontal lobes and autonoetic consciousness. Psychological Bulletin, 121,
331–354.
Williams, J. M., Barnhofer, T., Crane, C., Hermans, D., Raes, F., Watkins, E., et al. (2007).
Autobiographical memory specificity and emotional disorder. Psychological Bulletin, 133, 122–148.
Wilson, A. E., & Ross, M. (2003). The identity function of autobiographical memory:
Time is on our side. Memory, 11, 137–149.
Please cite this article in press as: Piolino, P., et al. Episodic autobiographical memories over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia (2009), doi:10.1016/j.neuropsychologia.2009.01.020